Pelecaniform Birds Research Articles

Worldwide Dispersion of Coccidia from Migratory Birds: First Report of Eimeria bazi Chauhan et Bhatia, 1970 (Eimeriidae) Outside Asia from Buff-Necked Ibises Theristicus caudatus (Boddaert, 1783) (Threskiornithidae) in South America.

Eimeria spp. are coccidian protozoan parasites of domestic and wild animals. Pelecaniform birds are hosts of some Eimeria spp., however, from the family Threskiornithidae only one eimerian species is recorded, Eimeria bazi Chauhan et Bhatia, 1970 which was described from red-naped ibises Pseudibis papillosa (Temminck, 1824) in India. In this study, in turn, this species is morphologically and molecularly identified from buff-necked ibises Theristicus caudatus (Boddaert, 1783) in Brazil. This study aimed to report E. bazi from buff-necked ibises T. caudatus in southeastern Brazil, revealing the worldwide distribution of this coccidian species, in addition to providing preliminary genotypic identification via sequencing of the mitochondrial cytochrome c oxidase subunit 1 (COI) gene. A total of 73 fecal samples were collected from a flock of buff-necked ibises, which remained on the campus of the Federal Rural University of Rio de Janeiro (Universidade Federal Rural do Rio de Janeiro-UFRRJ) from March 2019 to August 2020. Fecal samples were processed by the Sheather's method to recover oocysts. The morphological and morphometrical studies of the oocysts were performed using an optical microscope and graphic editing software. Molecular analysis was performed by sequencing of the COI gene, and the phylogenetic analysis was based in the neighbor-joining and maximum likelihood estimates. Forty-five fecal samples were positive for oocysts identified as E. bazi. This oocysts are ovoidal, 26.2 × 18.9μm, with smooth to slightly rough wall, c.1.7μm thick. Micropyle robust and protruding, sometimes with a polar body attached. Oocyst residuum absent, but one or two small polar granules are present. Sporocysts ovoidal to lemon-shaped, 14.2 × 8.7μm. The Stieda body is knob-like to rounded and sub-Stieda body is absent or vestigial. Sporocyst residuum is composed of granules often membrane-bound. Sporozoites are vermiform, with refractile bodies. This morphology was consistent with the original description of E. bazi from P. papillosa in India. Molecular analysis at the COI gene exhibited low similarity with coccidians sequenced for the same genic region deposited in GenBank, sitting E. bazi separately on the cladogram. The morphological and molecular studies support the identification of E. bazi from T. caudatus in South America, thus revealing the wide distribution of this eimerian species in the world provided by migratory birds and/or with intercontinental distribution.

A new species ofLimnofregata(Pelecaniformes:Fregatidae) from the Early Eocene Wasatch Formation of Wyoming: implications for palaeoecology and palaeobiology

AbstractA humerus and a coracoid from the Early Eocene Wasatch Formation in the Washakie Basin of south‐western Wyoming are the oldest materials (by ~2 million years) of the pelecaniformLimnofregata(Aves) and represent a new large species,Limnofregata hutchisonisp. nov. This fossil is the oldest known member of the frigatebird lineage. Other than its large size relative toLimnofregata azygosternonandL. hasegawai, the new material is very similar morphologically to other knownLimnofregataspecimens. The size of this new species is comparable to the largest living species (e.g.Fregata minorandFregata magnifiscens) and much larger than the two described species ofLimnofregata. This fossil indicates that the hard minimum date previously advocated for molecular calibration of the split between Fregatidae and Suloidea is an underestimate by approximately two million years. The presence of early pelecaniform bird lineages (represented byLimnofregataandMasillastega) in limnic ecosystems prior to their known occurrences in marine deposits/habitats appears to indicate that some clades of pelecaniform birds may have undergone an evolutionary transition from freshwater to marine habitats in a pattern reminiscent of what has been suggested during the evolution of pinnipeds or that their palaeoecology included broader niches ranging across a variety of aquatic habitats. That transition in habitat occupation and the origin of many of the characteristic biological aspects present in the crown frigatebird clade likely occurred during a significant temporal gap (> 45 million years) in the fossil record of the frigatebird lineage after these earliest occurrences in the Early Eocene and before the oldest records of the extantFregataspecies in the Pleistocene.

Beyond phylogeny: pelecaniform and ciconiiform birds, and long-term niche stability

Phylogenetic trees are a starting point for the study of further evolutionary and ecological questions. We show that for avian evolutionary relationships, improved taxon sampling, longer sequences and additional data sets are giving stability to the prediction of the grouping of pelecaniforms and ciconiiforms, thus allowing inferences to be made about long-term niche occupancy. Here we report the phylogeny of the pelecaniform birds and their water-carnivore allies using complete mitochondrial genomes, and show that the basic groupings agree with nuclear sequence phylogenies, even though many short branches are not yet fully resolved. In detail, we show that the Pelecaniformes (minus the tropicbird) and the Ciconiiformes (storks, herons and ibises) form a natural group within a seabird water-carnivore clade. We find pelicans are the closest relatives of the shoebill (in a clade with the hammerkop), and we confirm that tropicbirds are not pelecaniforms. In general, the group appears to be an adaptive radiation into an ‘aquatic carnivore’ niche that it has occupied for 60–70 million years. From an ecological and life history perspective, the combined pelecaniform–ciconiform group is more informative than focusing on differences in morphology. These findings allow a start to integrating molecular evolution and macroecology.

Fossil plotopterid seabirds from the Eo-Oligocene of the Olympic Peninsula (Washington State, USA): descriptions and functional morphology.

The plotopterids (Aves, Plotopteridae) were a group of extinct wing-propelled marine birds that are known from Paleogene-aged sediments (Eocene to Miocene), mostly around the Pacific Rim (especially Japan and the northwest coast of North America). While these birds exhibit a strikingly similar wing morphology to penguins (Spheniscidae), they also share derived characters with pelecaniform birds that are absent in penguins and exhibit apparently superficial similarities with auks (Alcidae: Charadriiformes). Despite quite an abundant fossil record, these birds have been little studied, and in particular their functional morphology remains little understood. Here we present osteological overviews of specimens from the northwest coast of Washington state (USA). We give an amended diagnosis for the well-represented North American genus, Tonsala Olson, 1980, describe a new large species, and examine the functional morphology of plotopterids showing that the ratio of humeral strength to femoral strength is quite low in one well-represented species Tonsala buchanani sp.nov., relative to both extant penguins and alcids. While the femoral strength of Tonsala buchanani is ‘penguin-grade’, its humeral strength is more ‘alcid-grade’. These results have implications for understanding the mode-of-locomotion of these extinct marine birds. Although not related to Spheniscidae, our descriptions and functional results suggest that Tonsala buchanani sustained similar loads in walking, but slightly lower humeral loads during swimming, than a modern penguin. This suggests a swimming mode that is more similar to living alcids, than to the highly-specialised locomotor strategy of living and fossil penguins.

Cross sectional geometry of the forelimb skeleton and flight mode in pelecaniform birds

Avian wing elements have been shown to experience both dorsoventral bending and torsional loads during flapping flight. However, not all birds use continuous flapping as a primary flight strategy. The pelecaniforms exhibit extraordinary diversity in flight mode, utilizing flapping, flap-gliding, and soaring. Here we (1) characterize the cross-sectional geometry of the three main wing bone (humerus, ulna, carpometacarpus), (2) use elements of beam theory to estimate resistance to loading, and (3) examine patterns of variation in hypothesized loading resistance relative to flight and diving mode in 16 species of pelecaniform birds. Patterns emerge that are common to all species, as well as some characteristics that are flight- and diving-mode specific. In all birds examined, the distal most wing segment (carpometacarpus) is the most elliptical (relatively high I(max) /I(min) ) at mid-shaft, suggesting a shape optimized to resist bending loads in a dorsoventral direction. As primary flight feathers attach at an oblique angle relative to the long axis of the carpometacarpus, they are likely responsible for inducing bending of this element during flight. Moreover, among flight modes examined the flapping group (cormorants) exhibits more elliptical humeri and carpometacarpi than other flight modes, perhaps pertaining to the higher frequency of bending loads in these elements. The soaring birds (pelicans and gannets) exhibit wing elements with near-circular cross-sections and higher polar moments of area than in the flap and flap-gliding birds, suggesting shapes optimized to offer increased resistance to torsional loads. This analysis of cross-sectional geometry has enhanced our interpretation of how the wing elements are being loaded and ultimately how they are being used during normal activities.

Forelimb skeletal morphology and flight mode evolution in pelecaniform birds

The total length and mid-shaft diameters of wing elements of 50 species of pelecaniform birds were examined to investigate how forelimb skeletal morphology varies with body size and flight mode within this group. Pelecaniforms were assigned to flight mode categories based on primary habitual behaviors (soar, flap-glide, continuous flap). Allometric and discriminant function analyses were conducted on wing element variables in both historical (using independent contrasts) and ahistorical contexts. Results of this study indicate that when phylogenetic relationships are taken into account, only the length of the ulna scales with positive allometry, whereas all other variables exhibit isometry. These results differ from the ahistorical allometric analysis. Discriminant function analysis (DFA) significantly separated the flight mode groups (Wilk's lambda=0.002, p<0.00001), with only six individuals from two species (out of n=284) misclassified. Results of historical canonical variates analysis supported the ahistorical DFA and identified two carpometacarpal (CMC) variables as important for separating the flight mode groups: dorsoventral CMC diameter and total CMC length. The carpometacarpus is that portion of the forelimb skeleton that serves as the attachment point for the primary flight feathers, and thus, that portion of the airfoil surface that mediates detailed flight control. Its morphology, more than any other element, reflects differences in flight mode in pelecaniforms. Results of this study indicate that, in pelecaniforms, wing bones generally exhibit isometry (with the exception of the ulna) and do possess specific morphologies reflective of the demands associated with different types of aerial locomotor specialization.

The importance of white on black: unmelanized plumage proportion predicts display complexity in birds

Animal ritualized displays have been classically viewed as behavioral characters that decrease signal ambiguity or that facilitate the evaluation of costly exhibitions. It has been shown that their prevalence and level of complexity across species can reflect phylogenetic relationships between them, but the adaptive function of these behavioral traits is poorly known. Here, I hypothesize that, given that the efficacy of visual displays basically depends on conspicuousness and level of performance, species with low levels of conspicuousness may be forced to perform more complex varieties of a given display to get the same signal efficiency than other more conspicuous species. Thus, the evolution of display complexity, considered as the level of exaggeration of ritualized movements, may be explained as an adaptive trait and not only by phylogenetic inertia. I illustrate and test this hypothesis with the case of black-and-white plumage patches of pelecaniform birds. As predicted, there was a negative correlation between level of complexity and species conspicuousness (proportion of unmelanized plumage) for two different social displays. This indicates that classical ideas on the adaptiveness of ritualized displays should be considered to understand the present variation in signal form across species, which sheds light on the evolution of multiple signals.

Multiple Cophylogenetic Analyses Reveal Frequent Cospeciation between Pelecaniform Birds and Pectinopygus Lice

Lice in the genus Pectinopygus parasitize a single order of birds (Pelecaniformes). To examine the degree of congruence between the phylogenies of 17 Pectinopygus species and their pelecaniform hosts, sequences from mitochondrial 12S rRNA, 16S rRNA, COI, and nuclear wingless and EF1-alpha genes (2290 nucleotides) and from mitochondrial 12S rRNA, COI, and ATPases 8 and 6 genes (1755 nucleotides) were obtained for the lice and the birds, respectively. Louse data partitions were analyzed for evidence of incongruence and evidence of long-branch attraction prior to cophylogenetic analyses. Host-parasite coevolution was studied by different methods: TreeFitter, TreeMap, ParaFit, likelihood-ratio test, data-based parsimony method, and correlation of coalescence times. All methods agree that there has been extensive cospeciation in this host-parasite system, but the results are sensitive to the selection of different phylogenetic hypotheses and analytical methods for evaluating cospeciation. Perfect congruence between phylogenies is not found in this association, probably as a result of occasional host switching by the lice. Errors due to phylogenetic reconstruction methods, incorrect or incomplete taxon sampling, or to different loci undergoing different evolutionary histories cannot be rejected, thus emphasizing the need for improved cophylogenetic methodologies.

Tertiary plotopterids (Aves, Plotopteridae) and a novel hypothesis on the phylogenetic relationships of penguins (Spheniscidae)

Plotopterids (Aves: Plotopteridae) are extinct wing-propelled diving birds which exhibit a strikingly similar wing morphology to penguins (Spheniscidae), but also share derived characters with pelecaniform birds that are absent in penguins. The similarities between Plotopteridae and Spheniscidae have hitherto been attributed to convergence, and plotopterids were considered to be most closely related to the pelecaniform Phalacrocoracidae (cormorants) and Anhingidae (anhingas). However, here I show that assignment of plotopterids to pelecaniform birds does not necessarily preclude them from being the sister taxon of penguins. Cladistic analysis of 68 morphological characters resulted in sister group relationship between Plotopteridae and Spheniscidae, and the clade (Plotopteridae + Spheniscidae) was shown to be the sister taxon of the Suloidea, i.e. a clade including Sulidae (boobies and gannets), Phalacrocoracidae, and Anhingidae. Derived characters are discussed which support this novel hypothesis. Paedomorphosis probably accounts for the absence of derived characters in penguins that are shared by Plotopteridae and members of the Steganopodes. Plotopterids exemplify the importance of fossil birds for analyzing the phylogenetic relationships of modern taxa that exhibit a highly apomorphic morphology.

Pseudo-homeosis in avian feet

Galis et al.'s analysis of the evolutionary constraints on vertebrate autopodal (manus–foot) development [1] includes questionable assertions of homeotic changes of digit identity (changes of identity of one digit into another) in the avian foot. The first example concerns the totipalmate condition that defines pelecaniform birds wherein all four pedal digits comprise a common foot web, with digit I being more forwardly directed than is typical of most birds where it is directed posteriorly. The authors state: ‘The fourth toe has moved forward’, but, in fact, it is the first toe. The other example is the foot of piciform birds, wherein both digits I and IV are directed posteriorly to produce a zygodactylous (yoke-toed) condition. Such a foot is well adapted for perching (puffbirds, etc.), climbing (woodpeckers), and running (roadrunners, etc.). The authors’ state: ‘In all cases, the extra opposed digit has been obtained by changing the form of the second digit into that of the first, opposable, digit’. In fact, in all zygodactylous avian feet, it is merely that digit IV has been repositioned. In the heterodactylous foot of trogons, a similar yoke-toed foot involves reversing digit II. There has never been any question concerning the identity of the digits in any of the above cases [2]: they correspond to their appropriate trochleae, connected with fidelity by their appropriate ligaments. Interestingly, owls, ospreys, touracos and mousebirds have a temporary or facultatively zygodactylous foot in which the fourth toe can be held either anteriorly or posteriorly during perching [2]. Galis et al. [1] offer no arguments to support their implication of homeotic changes in the evolution of the avian foot.

Pursuit plunging by northern gannets (Sula bassana) feeding on capelin (Mallotus villosus).

Northern gannets (Sula bassana) are considered to obtain prey usually by rapid, vertical, shallow plunge dives. In order to test this contention and investigate underwater foraging behaviour, we attached two types of data-logging systems to 11 parental northern gannets at Funk Island in the North-Wiest Atlantic. We documented, for the first time to the authors' knowledge, gannets performing long, flat-bottomed, U-shaped dives that involved underwater wing propulsion as well as rapid, shallow, V-shaped dives. The median and maximum dive depths and durations were 4.6 and 22.0 m and 8 and 38 s, respectively. Short, shallow dives were usually V-shaped and dives deeper than 8 m and longer than 10 s were usually U-shaped, including a period at constant depth (varying between 4 and 28s with median 8s). Diving occurred throughout the daylight period and deepest dives were performed during late morning. On the basis of motion sensors in the loggers and food collections from telemetered birds, we concluded that extended, deep dives were directed at deep schools of capelin, a small pelagic fish, and we hypothesized that V-shaped dives were aimed at larger, pelagic fishes and squids. Furthermore, these V-shaped dives allowed the birds to surprise their pelagic prey and this may be critical because the maximum swimming speeds of the prey species may exceed the maximum dive speeds of the birds.

Frigatebirds, Tropicbirds, and Ciconiida: Excesses of Confidence Probability

Because it is based on a significance test that takes the shape of the tree as given, the Rzhetsky/Nei Confidence Probability (CP) can attribute high “confidence” to groups with little or even literally no support. CP further overestimates confidence in that it takes no account of reliability of alignment, and it shows instability in that drastic changes in results can be produced by small changes in data. Instability can arise when alignment is uncertain, since different alignment strategies can lead to slightly different matrices. Parsimony jackknifing offers a more reliable and stable way of assessing support. To take ambiguities of alignment into account with parsimony jackknifing, we suggest “consensus” and “average” methods of summarizing jackknife results from several alignments. Reanalyzing 12S and 16S rRNA data on pelecaniform birds, we find that CP has overestimated support for the Ciconiida, for placing frigatebirds with condors, and for placing tropicbirds with cormorants.

Frigatebirds, Tropicbirds, and Ciconiida: Excesses of Confidence Probability

Because it is based on a significance test that takes the shape of the tree as given, the Rzhetsky/Nei Confidence Probability (CP) can attribute high “confidence” to groups with little or even literally no support. CP further overestimates confidence in that it takes no account of reliability of alignment, and it shows instability in that drastic changes in results can be produced by small changes in data. Instability can arise when alignment is uncertain, since different alignment strategies can lead to slightly different matrices. Parsimony jackknifing offers a more reliable and stable way of assessing support. To take ambiguities of alignment into account with parsimony jackknifing, we suggest “consensus” and “average” methods of summarizing jackknife results from several alignments. Reanalyzing 12S and 16S rRNA data on pelecaniform birds, we find that CP has overestimated support for the Ciconiida, for placing frigatebirds with condors, and for placing tropicbirds with cormorants.

The Structure of Preen Gland Waxes from Pelecaniform Birds Containing 3,7-Dimethyloctan-1-ol -an Active Ingredient against Dermatophytes

Abstract A biologically active principle has been isolated from the uropygial gland secretion of the gannet (Sula bassana) exhibiting growth inhibitory activity for Gram-positive bacteria, yeasts, moulds and, in particular, for dermatophytes.The feather lipids of this species consist of monoester waxes predominantly composed of 3,x-dimethylalkanols esterified with fatty acids belonging to homologous series of 2-and 3-methyl-, 2,x-and 3,x-dimethyl-as well as 2,x,y-and 3,x,y-trimethyl-substituted alkanoic acids. For chemosystematic reasons other pelecani­ form species (Pelecanus crispus, Pelecanus onocrotalus, Phaeton lepturus) and one gaviiform species (Gavia stellata) have also been analysed. The pattern of their preen wax constituents suggest to assume that the Pelecaniformes are polyphyletic with gannets and cormorants being closely related, whereas pelicans and tropic birds are different, both from the former and from each other. Pelicans resemble very much the grebes, while tropic birds seem to be more closely related to the charadriiform, alciform, and possibly to the gaviiform birds.

Eggshell structure in the Shoebill and pelecaniform birds: comparison with Hamerkop, herons, ibises, and storks

Scanning electron microscope investigation of eggshell structure supports earlier beliefs that the pelecaniform family assemblage is a natural group. All families of pelecaniform birds except the Phaethontidae show complete similarity in the structure of both the crystallized eggshell and the accessory (amorphous) material (cuticle and cover) located in the outer surface of the shell. Comparisons with other avian taxa (93 families of non-passeriform birds) show that in terms of eggshell structure, Scopus umbretta is an "advanced" ardeid and Balaeniceps rex a rather unusual pelecaniform. All these birds should form one large group with the Ardeidae and clearly distinguished from the Ciconiidae. The results of this investigation imply that, ultimately, the deposition of microglobular material in the cover of avian eggshell is subject to phylogenetic constraints rather than having an adaptive (ecological) cause.

Arboviruses in water birds (Ciconiiformes, Pelecaniformes) from Florida.

Sera from 360 ciconiform and pelecaniform birds collected in Florida (USA) from 1974 to 1990 were tested for serum neutralizing (SN) antibodies to eastern equine encephalitis (EEE), St. Louis encephalitis (SLE), and Everglades (EVE) viruses. Serum neutralizing antibodies to EEE virus were detected in 2%, to SLE virus in 7%, and to EVE virus in none of the samples. Pelecaniform birds (16%) had a higher antibody prevalence (P < 0.02) for SLE virus than did ciconiform birds (5%). Virus could not be isolated from 67 samples. Nestling birds with SN antibodies to both EEE and SLE viruses were found in both fresh water and marine colonies. Antibodies were more prevalent in adult and fledged juvenile birds than in nestlings.

The middle ear of the skull of birds: the Pelecaniformes and Ciconiiformes

The anatomy of the middle ear region of the skull is described for the families of the Avian orders Pelecaniformes and Ciconiiformes. Emphasis is placed on the foramina and paths of the nerves and blood vessels. The morphology of the basicranium and quadrate is also discussed. Comparative analyses of the characters are used to assess taxonomic conclusions. Extant Pelecaniformes consist of six families, four of which are monogenic: Phaethontidae, Pelecanidae, Anhingidae and Fregatidae; one is composed of two genera: Sulidae; and the last has three genera: Phalacrocoracidae. Several years ago a relationship was suggested which would ally the Phaethontidae and the Fregatidae. While these families share several non middle ear characters the anatomy of the middle ear is not compatible with any particular relationship. Indeed, several obvious differences are described. The data presented here are consistent with the idea that the Phaethontidae and the Fregatidae each form a separate group of Pelecaniform birds, with the rest of the families forming a third group. Several differences in the middle ear region of the species of Anhingidae suggest that the family may be composed of two genera. While sharing many Ciconiiform characters the Ciconiidae have been shown not to be as closely related to the Ardeidae as they are to other families of Ciconiiformes. In addition, evidence is presented to support the recent idea that the three species of ibis (I. ibis, I. cinereus and I. leucocephalus) be united within the genus Mycteria. Also supported is the notion that Balaeniceps is Pelecaniform in character, and not Ciconiiform.

Temperature Regulation in the Red-Tailed Tropic Bird and the Red-Footed Booby

This paper represents part of a study on the thermoregulatory responses of nesting sea birds to natural environmental conditions. The investigations were conducted on Midway Island. Our previous publications (Howell and Bartholomew, 1961a, 1961b) have dealt with Laysan and Black-footed albatrosses (Diomedea immutabilis and D. nigripes), Bonin Island Petrels (Pterodroma hypoleuca), and Wedge-tailed and Christmas Island shearwaters (Pufinus pacificus and P. nativitatis). Bailey (1956) gives a useful account of the natural history of these and other species found on Midway. In the course of visits to Midway Island in June and July, 1959 and 1960, we were able to obtain data on thermoregulation in the Red-tailed Tropic Bird (Phaethon rubricauda) and the Red-footed Booby (Sula sula). Aside from the work of Probine and Wodzicki (1955) on the Gannet (Sula bassana) and that of Bartholomew, Dawson, and O'Neill (1953) and Bartholomew and Dawson (1954) on pelicans (Pelecanus), we know of no quantitative studies on thermoregulation in pelecaniform birds.