Development syndromes in New World temperate and tropical songbirds.

We studied avian development in 49 to 153 species of temperate and tropical New World passerine birds to determine how growth rates, and incubation and nestling periods, varied in relation to other life-history traits. We collected growth data and generated unbiased mass and tarsus growth rate estimates (mass n = 92 species, tarsus n = 49 species), and measured incubation period (n = 151) and nestling period (n = 153), which we analyzed with respect to region, egg mass, adult mass, clutch size, parental care type, nest type, daily nest predation rate (DMR), and nest height. We investigated covariation of life-history and natural-history attributes with the four development traits after controlling for phylogeny. Species in our lowland tropical sample grew 20% (incubation period), 25% (mass growth rate), and 26% (tarsus growth rate) more slowly than in our temperate sample. Nestling period did not vary with respect to latitude, which suggests that tropical songbirds fledge in a less well-developed state than temperate species. Suboscine species typically exhibited slower embryonic and post-embryonic growth than oscine passerines regardless of their breeding region. This pattern of slow development in tropical species could reflect phylogenetic effects based on unknown physiological attributes. Time-dependent nest mortality was unrelated to nestling mass growth rate, tarsus growth rate, and incubation period, but was significantly associated with nestling period. This suggests that nest predation, the predominant cause of nest loss in songbirds, does not exert strong selection on physiologically constrained traits, such as embryonic and post-embryonic growth, among our samples of temperate and lowland tropical songbird species. Nestling period, which is evolutionarily more labile than growth rate, was significantly shorter in birds exposed to higher rates of nest loss and nesting at lower heights, among other traits. Differences in life-history variation across latitudes provide insight into how unique ecological characteristics of each region influence physiological processes of passerines, and thus, how they can shape the evolution of life histories. While development traits clearly vary with respect to latitude, trait distributions overlap broadly. Life-history and natural history associations differ for each development trait, which suggests that unique selective pressures or constraints influence the evolution of each trait.

Estimation of bone mineral density and breaking strength of laying hens based on scans of computed tomography for body composition analysis.

1. The objective of this study was to evaluate the prediction potential of a computer tomography (CT) data collection protocol for determining total body composition used for analysis of tibiotarsal bone quality features. 2. The CT image acquisition was performed on 54 healthy TETRA SL genotype laying hens at 90 weeks of age as well as in the 69th week of the egg production period in vivo and their tibiotarsal bones, ex vivo. 3. Breaking strengths and ash content of the tibiotarsal bones were estimated based on the calculated mineral density of skeletal and tibiotarsal bones by means of CT with an estimation accuracy R2 0.963 and 0.975, respectively. 4. In conclusion, the current investigation demonstrated that the acquisition protocol of CT for total-body composition analysis has a good potential for measuring the mineral status and breaking strength of the reference bone in laying hen.

Gestation length and racing performance in 115 Thoroughbred foals with incomplete tarsal ossification.

BACKGROUND: Incomplete ossification of the cuboidal bones of the carpus and tarsus in foals has the potential for significant consequences including chronic lameness and decreased athletic ability. OBJECTIVES: To determine if the degree of ossification of the cuboidal bones is associated with gestational length and if the diagnosis of incomplete ossification is a predictor of performance in Thoroughbred racehorses. STUDY DESIGN: Retrospective cohort study. METHODS: The medical records of Thoroughbred foals less than 90 days of age from 1994 to 2011 were examined and records containing tarsal radiographs identified. Radiographs of the tarsus were examined for signs of incomplete ossification and those that were incompletely ossified graded on a scale of 1-4 using a modification of a previously reported index, with Grade 1 being the least ossified and Grade 4 being the most. Gestational length was determined by examining breeding records and foaling dates reported to the Jockey Club. Race records for 2- and 3-year-old affected foals and their maternal siblings were obtained and compared. RESULTS: Foals with Grades 1 and 2 ossification were usually premature (gestation length <325 days), but Grades 3 and 4 were not. Foals with Grades 2 and 3 ossification were significantly less likely to race than their maternal siblings and Grades 1, 2, 3 and 4 foals earned less money. MAIN LIMITATIONS: A larger sample size of foals with Grade 1 ossification would increase the power of the study. Foals radiographed at an older age may have had lower ossification scores if radiographed earlier. CONCLUSIONS: Incomplete ossification, especially Grades 1 and 2, is associated with a short gestation length. Foals with Grades 2 and 3 incomplete ossification were less likely to race and Grades 1, 2 and 3 earned around $30,000 less than their maternal siblings.

No Trade-Offs between Lipid Stores and Structural Growth in Juvenile Zebra Finches Undergoing Nutritional Stress during Development.

Nutritional conditions during development can affect both structural growth and body fat deposition. Body size and body fat each have significant consequences for fitness, yet few studies have investigated how young birds balance resource allocation between structural growth and fat reserves. We raised zebra finches (Taeniopygia guttata) in consistently high- or low-food conditions until posthatch day 35 (PHD 35). From this age until PHD 62, half of the birds in each condition were switched to the other treatment, while the rest were maintained on the same conditions. Body mass, lean mass, body fat, and tarsus length were measured before (PHD 25) and after (PHD 55) nutritional independence. Precise measures of body composition were obtained noninvasively at both ages using quantitative magnetic resonance analysis. At PHD 25, birds in the high treatment had more body mass and lean mass than birds in the low treatment, but nutritional treatments did not affect body fat at this age. Unexpectedly, the strategic response of birds that experienced deteriorating food availability was to maintain body mass by increasing body fat and decreasing lean mass. Birds that experienced an improvement in food availability significantly increased body mass by increasing lean mass and not body fat. Birds maintained on a low diet throughout did not significantly increase body mass, lean mass, or body fat. Tarsus length was not affected by nutritional manipulations. These findings indicate that nutritional stress did not affect the relationship between skeletal growth and body fat deposition because lean mass, body fat, and tarsus length can be independently regulated at different developmental periods depending on nutritional conditions.

The zinc finger homeodomain-2 gene of Drosophila controls Notch targets and regulates apoptosis in the tarsal segments.

The development of the Drosophila leg is a good model to study processes of pattern formation, cell death and segmentation. Such processes require the coordinate activity of different genes and signaling pathways that progressively subdivide the leg territory into smaller domains. One of the main pathways needed for leg development is the Notch pathway, required for determining the proximo-distal axis of the leg and for the formation of the joints that separate different leg segments. The mechanisms required to coordinate such events are largely unknown. We describe here that the zinc finger homeodomain-2 (zfh-2) gene is highly expressed in cells that will form the leg joints and needed to establish a correct size and pattern in the distal leg. There is an early requirement of zfh-2 to establish the correct proximo-distal axis, but zfh-2 is also needed at late third instar to form the joint between the fourth and fifth tarsal segments. The expression of zfh-2 requires Notch activity but zfh-2 is necessary, in turn, to activate Notch targets such as Enhancer of split and big brain. zfh-2 is controlled by the Drosophila activator protein 2 gene and regulates the late expression of tarsal-less. In the absence of zfh-2 many cells ectopically express the pro-apoptotic gene head involution defective, activate caspase-3 and are positive for acridine orange, indicating they undergo apoptosis. Our results demonstrate the key role of zfh-2 in the control of cell death and Notch signaling during leg development.

Developmental competence and the induction of ectopic proboscises in Drosophila melanogaster.

Developmental competence is the response of a cell(s) to information. Determination of adult labial identity in Drosophila requires Proboscipedia (PB) and Sex combs reduced (SCR); however, co-ectopic expression of PB and SCR is not sufficient for induction of ectopic adult labial identity, because the developmental information supplied by PB and SCR is suppressed. The evolutionarily conserved LASCY, DYTQL, NANGE motifs, and the C-terminal domain of SCR are sequence elements that mediate some, or all, of the suppression of ectopic proboscis determination. Therefore, the developmentally competent primordial proboscis cells provide an environment devoid of suppression, allowing PB and SCR to determine proboscis identity. SCR derivatives lacking suppression sequences weakly induce ectopic proboscis transformations independently of PB, suggesting that SCR may be the activity required for induction of adult labial identity, as is the case for larval labial identity. A possible explanation for PB independence of SCR in determination of adult and embryonic labial identity is PB operates as a competence factor that switches SCR from determining T1 identity to labial identity during metamorphosis. Lastly, labial determination is not conserved between SCR and murine HOXA5, suggesting that SCR has acquired this activity during evolution.

Post-hatch heat warms adult beaks: irreversible physiological plasticity in Japanese quail.

Across taxa, the early rearing environment contributes to adult morphological and physiological variation. For example, in birds, environmental temperature plays a key role in shaping bill size and clinal trends across latitudinal/thermal gradients. Such patterns support the role of the bill as a thermal window and in thermal balance. It remains unknown whether bill size and thermal function are reversibly plastic. We raised Japanese quail in warm (30°C) or cold (15°C) environments and then at a common intermediate temperature. We predicted that birds raised in cold temperatures would develop smaller bills than warm-reared individuals, and that regulation of blood flow to the bill in response to changing temperatures would parallel the bill's role in thermal balance. Cold-reared birds developed shorter bills, although bill size exhibited 'catch-up' growth once adults were placed at a common temperature. Despite having lived in a common thermal environment as adults, individuals that were initially reared in the warmth had higher bill surface temperatures than cold-reared individuals, particularly under cold conditions. This suggests that blood vessel density and/or the control over blood flow in the bill retained a memory of early thermal ontogeny. We conclude that post-hatch temperature reversibly affects adult bill morphology but irreversibly influences the thermal physiological role of bills and may play an underappreciated role in avian energetics.

Nest predation risk and growth strategies of passerine species: grow fast or develop traits to escape risk?

Different body components are thought to trade off in their growth and development rates, but the causes for relative prioritization of any trait remains a critical question. Offspring of species at higher risk of predation might prioritize development of locomotor traits that facilitate escaping risky environments over growth of mass. We tested this possibility in 12 altricial passerine species that differed in their risk of nest predation. We found that rates of growth and development of mass, wings, and endothermy increased with nest predation risk across species. In particular, species with higher nest predation risk exhibited relatively faster growth of wings than of mass, fledged with relatively larger wing sizes and smaller mass, and developed endothermy earlier at relatively smaller mass. This differential development can facilitate both escape from predators and survival outside of the nest environment. Tarsus growth was not differentially prioritized with respect to nest predation risk, and instead all species achieved adult tarsus size by age of fledging. We also tested whether different foraging modes (aerial, arboreal, and ground foragers) might explain the variation of differential growth of locomotor modules, but we found that little residual variation was explained. Our results suggest that differences in nest predation risk among species are associated with relative prioritization of body components to facilitate escape from the risky nest environment.

[Postnatal growth patterns in eight species of herons and egrets (Ciconiiformes: Ardeidae)]. / Patrones de crecimiento postnatal en ocho especies de garzas (Ciconiiformes: Ardeidae).

Avian postnatal growth has received considerable attention and its ecological implications have been deeply analyzed. In this current paper, I describe the patterns of culmen and tarsus growth, as well as of weight gain patterns in eight species of herons and egrets (Aves: Ardeidae) found in the Birama Swamp in Eastern Cuba. Between 1998 and 2006,714 nestlings of the following species were measured every two days: Butorides virescens, Bubulcus ibis, Egretta thula, E. tricolor, E. caerulea, E. rufescens, Ardea alba and Nycticorax nycticorax. Logistic and Gompertz equations were adjusted to data using non-lineal regression models with adult values as the asymptote. For each species, the following were determined and recorded: growth rate, age at inflexion, instantaneous growth rates at each age interval, and time taken to reach 90% of adult size. Reported hatchling sizes were similar in other localities, with a variation coefficient ranging between 10-19%. At hatch, each species exhibited differing sizes relative to adult values. In all cases, Gompertz equations were best fitted to explain more variance and lesser residuals. Rates of weight change and tarsus growth were alometrically related to the log of adult weight. Two main growth processes were identified: a physical extension in dimensions of each measurement reflecting inter-specific morphometric differences, and a lineal increase of the growth period from Green Heron to Great Egret. The Black-crowned Night Heron, Cattle Egret and Reddish Egret exhibited some unique measurement characteristics in comparison to the remaining members of the family. All results support the hypothesis that hypermorphosis, as the main evolutionary process in the microevolution of Ardeidae, is caused by a delayed final moment of growth.

Patrones de crecimiento postnatal en ocho especies de garzas (Ciconiiformes: Ardeidae)

Postnatal growth patterns in eight species of herons and egrets (Ciconiiformes: Ardeidae). Avian postnatal growth has received considerable attention and its ecological implications have been deeply analyzed. In this current paper, I describe the patterns of culmen and tarsus growth, as well as of weight gain patterns in eight species of herons and egrets (Aves: Ardeidae) found in the Birama Swamp in Eastern Cuba. Between 1998 and 2006, 714 nestlings of the following species were measured every two days: Butorides virescens, Bubulcus ibis, Egretta thula, E. tricolor, E. caerulea, E. rufescens, Ardea alba and Nycticorax nycticorax. Logistic and Gompertz equations were adjusted to data using non-lineal regression models with adult values as the asymptote. For each species, the following were determined and recorded: growth rate, age at inflexion, instantaneous growth rates at each age interval, and time taken to reach 90% of adult size. Reported hatchling sizes were similar in other localities, with a variation coefficient ranging between 10-19%. At hatch, each species exhibited differing sizes relative to adult values. In all cases, Gompertz equations were best fitted to explain more variance and lesser residuals. Rates of weight change and tarsus growth were alometrically related to the log of adult weight. Two main growth processes were identified: a physical extension in dimensions of each measure ment reflecting inter-specific morphometric differences, and a lineal increase of the growth period from Green Heron to Great Egret. The Black-crowned Night Heron, Cattle Egret and Reddish Egret exhibited some unique measurement characteristics in comparison to the remaining members of the family. All results support the hypothesis that hypermorphosis, as the main evolutionary process in the microevolution of Ardeidae, is caused by a delayed final moment of growth. Rev. Biol. Trop. 59 (2): 771-787. Epub 2011 June 01.

El crecimiento en aves forma parte de las estrategias reproductivas y su implicación ecológica ha sido profundamente debatida. En este trabajo se describe el crecimiento del pico, peso y tarso de ocho garzas (Aves: Ardeidae) en la ciénaga de Birama, Cuba. Para ello, entre 1998-2006, se midieron en días alternos un total de 714 pichones de Butorides virescens, Bubulcus ibis, Egretta thula, E. tricolor, E. caerulea, E. rufescens, Ardea alba y Nycticorax nycticorax, durante sus dos primeras semanas de vida. Se hicieron ajustes a las curvas Logística y de Gompertz y se usó regresiones no lineales y valores adultos como asíntotas, además se determinaron las variables que describenel crecimiento. El tamaño de los pichones al eclosionar fue similar al encontrado en otras localidades, con CV entre 10-19% y diferencias relativas al tamaño adulto. Las ecuaciones de Gompertz tuvieron menos residuos en todos los casos. Entonces, se identificaron dos procesos fundamentales de extensión en el crecimiento de cada estructura: uno físico y otro de duración, entre B. virescens y E. alba. Nycticorax, B. ibis y E. rufescens mostraron variaciones que los diferenciaron del resto. Los resultados apoyan la hipótesis de la microevolución de Ardeidae por hipermorfosis, por un retardo en el momento final del crecimiento.

Variation of a carotenoid-based trait in relation to oxidative stress and endocrine status during the breeding season in the Eurasian kestrel: a multi-factorial study.

Carotenoid-based skin colorations vary seasonally in many bird species and are thought to be honest sexually selected signals. In order to provide more insight in the potential signal function and underlying mechanisms of such colorations we here quantified patterns of variation of leg coloration in adult male and female Eurasian kestrels (Falco tinnunculus tinnunculus) over the breeding season, and evaluated the relationship between coloration and levels of carotenoids, androgens and estrogens, oxidative damage and plasma non-enzymatic antioxidant capacity. We studied both reproducing wild and non-reproducing captive birds to test for the effect of diet and breeding effort. Males were more colored than females only during mating, and independently of diet, suggesting that leg-color is a sexually selected trait. Seasonal variation in leg color was associated with circulating carotenoids, but concentrations of these molecules were not related to antioxidant capacity, body condition or oxidative damage. These results indicate that carotenoid-based colorations may not be an honest signal of health status in this species. Production of carotenoid rich eggs coincided with low levels of circulating carotenoids in females, indicating that carotenoids might be a limited resource for laying female kestrels. Finally, young rearing males had higher levels of oxidative damage than females, and wild birds of both sexes had higher levels of these parameters than captive birds. These results may indicate that parental effort and physical activity are costly, independently from hormonal status. Since androgens did not explain carotenoid variation we suggest that multiple interacting factors can regulate carotenoid levels along the season.

Tarsus determination in Drosophila melanogaster.

Arista versus tarsus determination is well investigated in Drosophila, yet it remains unresolved whether Antennapedia (ANTP) cell autonomously or noncell autonomously determines tarsus identity and whether Sex combs reduced (SCR) is the HOX protein required for normal tarsus determination. Three observations rule out a cell autonomous role for ANTP in tarsus determination. (i) Clonal ectopic overexpression of ANTP did not repress the expression of the arista determining protein Homothorax (HTH) in early 3rd stadium antennal imaginal discs. (ii) Clonal ectopic expression of ANTP did not transform the arista to a tarsus. (iii) Ectopic overexpression of ANTP, Labial (LAB), Deformed (DFD), SCR, Ultrabithorax (UBX), Abdominal-A (ABD-A), or Abdominal-B (ABD-B), using the dppGAL4 driver, resulted in arista-to-tarsus transformations, and repressed HTH/Extradenticle (EXD) activity noncell autonomously in early 3rd stadium antennal imaginal discs. SCR may not be the HOX protein required for normal tarsus determination, because co-ectopic expression of Proboscipedia (PB) inhibited the arista-to-tarsus transformations induced by ectopic expression of DFD, SCR, ANTP, UBX, ABD-A, and ABD-B. The proposal that SCR is the HOX protein required for normal tarsus determination is dependent on SCR being the sole target of PB suppression, which is not the case. Therefore, the possibility exists that normal tarsus determination is HOX independent.

Development of the skeleton and feathers of dusky parrots (Pionus fuscus) in relation to their behaviour.

A clutch of five dusky parrots (Pionus fuscus) was observed from hatching to fully grown. They were examined radiographically from 16 to 45 days of age, a few days before the cessation of bone growth, and the development of their feathers and their behaviour were also studied. It was observed that when growing birds were removed from the nest and placed singly on a flat surface they would stand up and walk about until restrained; normally these birds would move very little and lie in an intertwined huddle that supported their relatively weak growing skeletons. At 50 days old they would climb to the nest entrance, retreating if scared. From day 51 the parrots flapped their wings vigorously inside the nest box, and they emerged at 53 days old when nearly all their large feathers had finished growing. These findings may help to explain the high rate of juvenile osteodystrophy in hand-reared parrots; premature exercise could lead to pathological deformity of the long bones, especially the major weight-bearing bone, the tibiotarsus.

Sex-biased hatching order and adaptive population divergence in a passerine bird.

Most species of birds can lay only one egg per day until a clutch is complete, and the order in which eggs are laid often has strong and sex-specific effects on offspring growth and survival. In two recently established populations of the house finch (Carpodacus mexicanus) in Montana and Alabama, breeding females simultaneously adjusted the sex and growth of offspring in relation to their position in the laying order, thereby reducing the mortality of sons and daughters by 10 to 20% in both environments. We show experimentally that the reduction in mortality is produced by persistent and sex-specific maternal effects on the growth and morphology of offspring. These strong parental effects may have facilitated the rapid adaptive divergence among populations of house finches.

Does the mechanical milieu associated with high-speed running lead to adaptive changes in diaphyseal growing bone?

Exercise during growth can be important for attaining optimal bone mass. High-intensity long-duration protocols, however, can have detrimental effects on immature bone morphology and mechanics. The underlying mechanisms are poorly understood. Here, we quantified the mechanical environment of the middiaphyseal rooster tarsometatarsus during high-speed running and examined whether short bouts of this exercise-related mechanical milieu can induce positive changes in cortical bone morphology, mechanics, and mineral ash content. At 9 weeks of age, roosters were assigned to controls (n = 9) and runners (n = 8). Treadmill running was applied in loading sessions of 5 min, three times per day (approximately 2600 cycles/day) for 8 weeks. Both controls and runners received double-fluorochrome labels during weeks 3 and 8 of the protocol. Middiaphyseal distributions of tarsometatarsal longitudinal normal strain, strain rate, and strain gradients engendered by walking and running were determined via in vivo strain gauges. Compared with walking, running elevated mean peak strain magnitude by 19%, peak strain rates by 136%, and peak strain gradients by approximately 18%. After 8 weeks of running, middiaphyseal areal and mechanical properties and normalized ash weight were no different between runners and controls. Transient and focal reductions in periosteal mineral apposition rates occurred during the exercise protocol. Our current data suggest that reducing the number of loading cycles can mitigate the adverse response previously observed in this model with long-duration running. This study also supports the tenet that the exercise-generated mechanical milieu must differ substantially from the habitual milieu to induce significant adaptations.

An experimental study on the effects of polymorphiasis in common eider ducklings.

Eight common eider (Somateria mollissima) ducklings were experimentally infected from 1 June through 13 June, 1995 with acanthocephalans (Polymorphus minutus) by allowing the birds to feed on Gammarus spp. (Gammarus oceanicus, G. salinus, G. zaddachi, and G. lacustris) containing acanthocephalan cystacanths. Uninfected Gammarus spp. were fed to a control group of seven ducklings. No mortality of ducklings occurred during the experiment. However, the infected ducklings gained weight more slowly than the control birds. After the 2 wk study period, the mean serum concentrations of total protein, albumin, beta-globulin, gamma-globulin, fructosamine and creatine kinase were lower in the infected group than in the controls. The mean (+/-SE) number of acanthocephalans in the intestine of the infected ducklings was 21 (+/-4). The parasites were attached to the mucosa of the posterior small intestine of the infected ducklings with a mixed inflammatory reaction consisting of heterophils and mononuclear lymphocytes surrounding the attachment sites.

Control of distal antennal identity and tarsal development in Drosophila by spineless-aristapedia, a homolog of the mammalian dioxin receptor.

We report the molecular characterization of the spineless (ss) gene of Drosophila, and present evidence that it plays a central role in defining the distal regions of both the antenna and leg. ss encodes the closest known homolog of the mammalian dioxin receptor, a transcription factor of the bHLH-PAS family. Loss-of-function alleles of ss cause three major phenotypes: transformation of distal antenna to leg, deletion of distal leg (tarsal) structures, and reduction in size of most bristles. Consistent with these phenotypes, ss is expressed in the distal portion of the antennal imaginal disc, the tarsal region of each leg disc, and in bristle precursor cells. Ectopic expression of ss causes transformation of the maxillary palp and distal leg to distal antenna, and induces formation of an ectopic antenna in the rostral membrane. These effects indicate that ss plays a primary role in specifying distal antennal identity. In the tarsus, ss is expressed only early, and is required for later expression of the tarsal gene bric à brac (bab). Ectopic expression causes the deletion of medial leg structures, suggesting that ss plays an instructive role in the establishment of the tarsal primordium. In both the antenna and leg, ss expression is shown to depend on Distal-less (Dll), a master regulator of ventral appendage formation. The antennal transformation and tarsal deletions caused by ss loss-of-function mutations are probably atavistic, suggesting that ss played a central role in the evolution of distal structures in arthropod limbs.

Appearance of ossification centers of the lower arm, wrist, lower leg, and ankle in immature orangutans and chimpanzees with an assessment of the relationship of ossification to dental development.

This study examines the appearance of the secondary ossification centers in the lower arms, wrists, lower legs, and ankles of a cross-sectional sample of 20 infant orangutans and chimpanzees (15 of known age). The number of tarsal and carpal centers is analyzed relative to the degree of M1 development and the weight of individual animals. Variation in the appearance of these ossification centers is discussed relative to these variables and others. In addition, a sequence of appearance is established for the carpal and tarsal ossification centers in the orangutan and data is presented on the status of these centers in a fetal and newborn gorilla. Study results indicate that 1) there is variation in the number of secondary epiphyses present in animals of similar ages; 2) tarsal ossification is completed prior to carpal ossification in the orangutan; 3) there are indications of a relationship between weight and the number of ossification centers present in animals of similar age; and 4) there appears to be no evidence of specific relationships between carpal and tarsal development and M1 development.