Mathew L. Berg

Avian retinal oil droplets: dietary manipulation of colour vision?

Avian vision is highly developed, with bird retinas containing rod and double-cone photoreceptors, plus four classes of single cones subserving tetrachromatic colour vision. Cones contain an oil droplet, rich in carotenoid pigments (except VS/ultraviolet-sensitive cones), that acts as a filter, substantially modifying light detected by the photoreceptor. Using dietary manipulations, we tested the effects of carotenoid availability on oil droplet absorbance properties in two species: Platycercus elegans and Taeniopygia guttata. Using microspectrophotometry, we determined whether manipulations affected oil droplet carotenoid concentration and whether changes would alter colour discrimination ability. In both species, increases in carotenoid concentration were found in carotenoid-supplemented birds, but only in the double cones. Magnitudes of effects of manipulations were often dependent on retinal location. The study provides, to our knowledge, the first experimental evidence of dietary intake over a short time period affecting carotenoid concentration of retinal oil droplets. Moreover, the allocation of carotenoids to the retina by both species is such that the change potentially preserves the spectral tuning of colour vision. Our study generates new insights into retinal regulation of carotenoid concentration of oil droplets, an area about which very little is known, with implications for our understanding of trade-offs in carotenoid allocation in birds.

Ultraviolet-sensitive vision in long-lived birds

Long-term exposure to ultraviolet (UV) light generates substantial damage, and in mammals, visual sensitivity to UV is restricted to short-lived diurnal rodents and certain marsupials. In humans, the cornea and lens absorb all UV-A and most of the terrestrial UV-B radiation, preventing the reactive and damaging shorter wavelengths from reaching the retina. This is not the case in certain species of long-lived diurnal birds, which possess UV-sensitive (UVS) visual pigments, maximally sensitive below 400 nm. The Order Psittaciformes contains some of the longest lived bird species, and the two species examined so far have been shown to possess UVS pigments. The objective of this study was to investigate the prevalence of UVS pigments across long-lived parrots, macaws and cockatoos, and therefore assess whether they need to cope with the accumulated effects of exposure to UV-A and UV-B over a long period of time. Sequences from the SWS1 opsin gene revealed that all 14 species investigated possess a key substitution that has been shown to determine a UVS pigment. Furthermore, in vitro regeneration data, and lens transparency, corroborate the molecular findings of UV sensitivity. Our findings thus support the claim that the Psittaciformes are the only avian Order in which UVS pigments are ubiquitous, and indicate that these long-lived birds have UV sensitivity, despite the risks of photodamage.

The evolution of plumage colouration in parrots: a review

Abstract The plumages of parrots provide some of the most striking colouration in nature. We summarise the diversity of mechanisms producing colour in parrots and the current evidence for the adaptive significance of variation in the colour of parrot plumages. Only recently have detailed studies begun to unravel the mechanisms of their colour-production and colour-vision systems. Parrots produce much of their plumage colouration through a unique suite of pigments (psittacofulvins), or through a feather tissue nanostructure that results in coherent scattering of light, or a combination of the two (producing green). Psittacofulvins are found nowhere else in nature, and may even generate fluorescence in many parrot species. Compared with other avian taxa, the adaptive significance of parrot plumage colouration remains poorly understood, although some studies suggest that plumage colouration may form important sexual signals and may be used in mate-choice by several species. There is evidence to suggest that parrot colouration can be subject to both environmental and genetic control. We emphasise that parrots offer a distinctive and useful colouration system for further study. Further research is required to unravel how the dramatic colour patterns of parrots evolved, and what roles colour signals may play in the life histories of parrots.

Learned Vocal Variation Is Associated with Abrupt Cryptic Genetic Change in a Parrot Species Complex

Contact zones between subspecies or closely related species offer valuable insights into speciation processes. A typical feature of such zones is the presence of clinal variation in multiple traits. The nature of these traits and the concordance among clines are expected to influence whether and how quickly speciation will proceed. Learned signals, such as vocalizations in species having vocal learning (e.g. humans, many birds, bats and cetaceans), can exhibit rapid change and may accelerate reproductive isolation between populations. Therefore, particularly strong concordance among clines in learned signals and population genetic structure may be expected, even among continuous populations in the early stages of speciation. However, empirical evidence for this pattern is often limited because differences in vocalisations between populations are driven by habitat differences or have evolved in allopatry. We tested for this pattern in a unique system where we may be able to separate effects of habitat and evolutionary history. We studied geographic variation in the vocalizations of the crimson rosella (Platycercus elegans) parrot species complex. Parrots are well known for their life-long vocal learning and cognitive abilities. We analysed contact calls across a ca 1300 km transect encompassing populations that differed in neutral genetic markers and plumage colour. We found steep clinal changes in two acoustic variables (fundamental frequency and peak frequency position). The positions of the two clines in vocal traits were concordant with a steep cline in microsatellite-based genetic variation, but were discordant with the steep clines in mtDNA, plumage and habitat. Our study provides new evidence that vocal variation, in a species with vocal learning, can coincide with areas of restricted gene flow across geographically continuous populations. Our results suggest that traits that evolve culturally can be strongly associated with reduced gene flow between populations, and therefore may promote speciation, even in the absence of other barriers.

Does the ring species concept predict vocal variation in the crimson rosella, Platycercus elegans, complex?

Vocal variation may be important in population divergence. We studied geographical variation in contact calls of parrots of the crimson rosella, Platycercus elegans, complex, which is characterized by striking geographical plumage coloration variation. This complex has long been considered a rare example of a ring species (where two divergent forms coexist in sympatry but are connected by a chain of intermediate populations forming a geographical ring). We tested whether contact call variation is consistent with the ring species hypothesis. We recorded calls throughout the ring, including several sites from the three main population groups forming the ring and interfaces between them. We analysed duration, peak frequency, fundamental frequency and frequency modulation. We found significant differences, particularly in fundamental frequency and frequency modulation, at multiple biogeographical scales ranging from local populations to subspecies level. Discriminant function analyses showed some populations could be reliably discriminated from call structure. However, our results provided little support for three key predictions of the ring species hypothesis: (1) calls of the terminal, most divergent forms were not significantly different in three of the four acoustic variables, and differences did not appear to be maintained in sympatry, (2) phenotypically/geographically intermediate populations were not characterized by intermediate calls, and (3) call variation was not concordant with geographical sequence around the ring from one terminal form to the other. Our results underscore the emerging view that the evolutionary histories and phenotypic variability of many long-held ring species may be inadequately described by the ring species hypothesis and require alternative explanations.

Phylogenetic analysis of beak and feather disease virus across a host ring-species complex

Significance The roles of disease and species hybridization in maintaining biodiversity are of wide interest, yet are rarely studied simultaneously in wild populations. Using genomic analysis of beak and feather disease virus in an avian ring-species complex, Platycercus elegans, to our knowledge we find viral phylogenetic structure analogous to Mayr’s ring-species hypothesis for the first time in any pathogen. Across 8 y, the host’s viral prevalence and infection load was lower in hybrid birds and in phenotypically intermediate subspecies. Viral genetic variation did not explain host prevalence or infection load, supporting conclusions that the evolved host response is more important. We show how host–species complexes and viral genomic analyses can provide insight into maintenance of biodiversity. Pathogens have been hypothesized to play a major role in host diversity and speciation. Susceptibility of hybrid hosts to pathogens is thought to be a common phenomenon that could promote host population divergence and subsequently speciation. However, few studies have tested for pathogen infection across animal hybrid zones while testing for codivergence of the pathogens in the hybridizing host complex. Over 8 y, we studied natural infection by a rapidly evolving single-strand DNA virus, beak and feather diseases virus (BFDV), which infects parrots, exploiting a host-ring species complex (Platycercus elegans) in Australia. We found that host subspecies and their hybrids varied strikingly in both BFDV prevalence and load: both hybrid and phenotypically intermediate subspecies had lower prevalence and load compared with parental subspecies, while controlling for host age, sex, longitude and latitude, as well as temporal effects. We sequenced viral isolates throughout the range, which revealed patterns of genomic variation analogous to Mayr’s ring-species hypothesis, to our knowledge for the first time in any host–pathogen system. Viral phylogeny, geographic location, intraspecific host density, and parrot community diversity and composition did not explain the differences in BFDV prevalence or load between subpopulations. Overall, our analyses suggest that functional host responses to infection, or force of infection, differ between subspecies and hybrids. Our findings highlight the role of host hybridization and clines in altering host–pathogen interactions, dynamics that can have important implications for models of speciation with gene flow, and offer insights into how pathogens may adapt to diverging host populations.

How parrots see their colours: novelty in the visual pigments of Platycercus elegans.

SUMMARY Intraspecific differences in retinal physiology have been demonstrated in several vertebrate taxa and are often subject to adaptive evolution. Nonetheless, such differences are currently unknown in birds, despite variations in habitat, behaviour and visual stimuli that might influence spectral sensitivity. The parrot Platycercus elegans is a species complex with extreme plumage colour differences between (and sometimes within) subspecies, making it an ideal candidate for intraspecific differences in spectral sensitivity. Here, the visual pigments of P. elegans were fully characterised through molecular sequencing of five visual opsin genes and measurement of their absorbance spectra using microspectrophotometry. Three of the genes, LWS, SW1 and SWS2, encode for proteins similar to those found in other birds; however, both the RH1 and RH2 pigments had polypeptides with carboxyl termini of different lengths and unusual properties that are unknown previously for any vertebrate visual pigment. Specifically, multiple RH2 transcripts and protein variants (short, medium and long) were identified for the first time that are generated by alternative splicing of downstream coding and non-coding exons. Our work provides the first complete characterisation of the visual pigments of a parrot, perhaps the most colourful order of birds, and moreover suggests more variability in avian eyes than hitherto considered.

Fruitful use of bioacoustic alarm stimuli as a deterrent for Crimson Rosellas (Platycercus elegans)

Abstract Birds cause considerable damage to horticultural crops in Australia each year. The playback of species-specific bioacoustic alarm stimuli has been one of the most promising methods suggested to deal with bird-problems. However, no published studies have tested this method on species of parrots, one of the main avian pests of crops in Australia and globally. Furthermore the effectiveness of this method might be reduced if alarm calls were played back that came from a non-local population. The Crimson Rosella species complex (Platycercus elegans), a parrot with considerable acoustic variation throughout its range, is considered a pest species of several commercial fruit crops. This study tested whether alarm calls from Crimson Rosellas were effective in reducing the activity of Rosellas in apple orchards. Three groups of bioacoustic stimuli were compared: control stimuli, local alarm calls and non-local alarm calls. Our results indicate that the playback of alarm calls from Crimson Rosellas is effective in reducing the activity of Rosellas in orchards over the period of study, and we did not find any difference between the use of local and non-local alarm calls. Our study suggests that playback of alarm calls may be an effective deterrent of rosellas over a broad distribution, at least for short-to medium-term use.

Prevalence of beak and feather disease virus in wild Platycercus elegans: comparison of three tissue types using a probe-based real-time qPCR test

Abstract. The detection of avian viruses in wild populations has considerable conservation implications. For DNA-based studies, feathers may be a convenient sample type for virus screening and are, therefore, an increasingly common technique. This is despite recent concerns about DNA quality, ethics, and a paucity of data comparing the reliability and sensitivity of feather sampling to other common sample types such as blood. Alternatively, skeletal muscle tissue may offer a convenient sample to collect from dead birds, which may reveal viraemia. Here, we describe a probe-based quantitative real-time PCR for the relative quantification of beak and feather disease virus (BFDV), a pathogen of serious conservation concern for parrots globally. We used this method to test for BFDV in wild crimson rosellas (Platycercus elegans), and compared three different sample types. We detected BFDV in samples from 29 out of 84 individuals (34.5%). However, feather samples provided discordant results concerning virus presence when compared with muscle tissue and blood, and estimates of viral load varied somewhat between different sample types. This study provides evidence for widespread infection of BFDV in wild crimson rosellas, but highlights the importance of sample type when generating and interpreting qualitative and quantitative avian virus data.

How does nest box temperature affect nestling growth rate and breeding success in a parrot

Abstract Climate change is predicted to affect many species by reducing range, habitat suitability and breeding success. Cavity-nesting species, already threatened by deforestation and declining natural hollows, may be particularly at risk because they are limited in nest-site location, and climatic alterations may further reduce usability of natural cavities. It is therefore essential to determine how cavity-users may be affected. We recorded internal nest-box temperatures and modelled the relationships of four temperature parameters (relating to mean temperature, variability in temperature, low temperature extremes and high temperature extremes) with breeding success and nestling growth in an Australian cavity-nesting parrot, the Crimson Rosella (Platycercus elegans). We found that less extreme low temperatures resulted in heavier nestlings; however, higher mean temperatures tended to result in lighter nestlings. Greater temperature variability tended to reduce fledging success; however, no temperature variables had a clear effect on clutch size or hatching success. Our findings indicate that there may be a complex relationship between nestling growth and temperature, and although less extreme cold temperatures may benefit nestlings, continued increases in mean temperature and variability may have negative consequences.