The endangered cape parrot really is a distinct species, according to a newly-published molecular study -- a finding that could impact conservation decisions and strategies in South Africa for decades to come

The taxonomy of the Cape parrot, Poicephalus robustus robustus, has long been controversial, particularly amongst conservation biologists and policymakers. But today, a team of South African scientists published a study that agrees with previously published morphological, ecological, and behavioural assessments indicating that this taxon should be elevated to full species status. In this study, the authors analysed genetic data from five Poicephalus parrot species and found that the Cape parrot is genetically distinct from all of its closest relatives. This taxonomic revision could facilitate better planning and implementation of international and local conservation management strategies for protecting this critically endangered parrot.

Ecology and natural history suggest Cape parrots are distinct taxa

The genus Poicephalus is a group of smallish- to medium-sized parrots that have a chunky build, short broad tails, stout beaks and relatively large heads. Their size combined with their playfulness and peaceful and confiding personalities have made several Poicephalus parrot species into popular pets worldwide.

Poicephalus are the most species-rich and widely-distributed group of parrots in Sub-Saharan Africa. There are nine species of Poicephalus, and they are divided into two lineages, or clades:

the P. robustus clade, which includes the Cape parrot, P. robustus, and the red-fronted parrot, P. gulielmi

the P. meyeri clade, which includes the yellow-faced parrot, P. flavifrons, Senegal parrot, P. senegalus, red-bellied parrot, P. rufiventrisi, Niam-niam parrot, P. crassus, brown-headed parrot, P. cryptoxanthus, Meyer’s parrot, P. meyeri and Ruppell’s parrot, P. rueppellii



Of these, several species (P. robustus, P. gulielmi, P. senegalus, P. flavifrons and P. meyeri) are further divided into a number of subspecies.

Within the P. robustus clade, the brown-necked parrot, P. r. fuscicollis, is found in Red Mangrove forests, mature wooded savannah and palm woodlands, and is now mostly restricted to the Gambia, thanks to habitat destruction. The grey-headed parrot, P. r. suahelicus, occurs in a wide variety of woodland habitats and is widely distributed across portions of several southeastern African nations. In contrast, the Cape parrot, P. r. robustus, is a habitat specialist that is almost exclusively restricted to the Afrocarpus/Podocarpus forests of southern Africa (Figure 1):

Facebook Twitter Pinterest Figure 1. Distribution map of the Poicephalus species (and P. robustus subspecies) included in the study (maps redrawn from Perrin 2012, photos used with permission from Cyril Laubscher). Illustration: Cyril Laubscher/Willem G. Coetzer et al./PLoS ONE 2015

Since there are three geographically separated yet closely related populations of the Cape parrot, Poicephalus robustus, there are conflicting interpretations for how these taxa should be formally classified. Previous research indicates that these three forms differ in habitat, body size, morphology, vocalisations and plumage patterns. Further, even in the Limpopo Province of South Africa where the distributions of P. r. robustus and P. r. suahelicus overlap, there is strong evidence that these two taxa are ecologically separated by habitat and altitude. The Cape parrot is limited to mixed Afrocarpus/Podocarpus mistbelt forests above 1000 metres whilst the grey-headed parrot is found in mixed woodland habitats below 800 metres (doi:10.2989/00306520509485493 ). Moreover, the Cape parrot breeds at a different time of the year, and it is a dietary specialist that predominantly feeds on Afrocarpus/Podocarpus fruits, whereas the grey-headed parrot has a more eclectic diet.

Based upon this wealth of data, most ornithologists agree that the temperate, montane forest dwelling Cape parrot, P. r. robustus, is a distinct species from the two savanna forms, the brown-necked parrot, P. r. fuscicollis of West Africa and the grey-headed parrot, P. r. suahelicus, of eastern and southern Africa. (For these reasons, aviculturists sometimes refer to the savannah forms as “un-Cape parrots”.)

Aside from that, because the two “un-Cape” parrots are known to occur in different types of tropical savanna, some authorities think detailed investigations into plumage variations, ecology and genetics will ultimately reveal that P. robustus actually comprises three separate species. The evidence supporting this view include the separate, non-overlapping geographic distributions, distinct biomes and dietary preferences for the three forms. This view is further supported by limited data on mitochondrial DNA differences between the three taxa.

DNA analyses indicate Cape parrots are distinct taxa

Clearly, more DNA work was needed to better resolve this contentious issue. Together with his colleagues, Willem Coetzer, a doctoral candidate in conservation genetics at the University of KwaZulu-Natal, went in to the field to capture wild P. robustus and collect a small blood sample to obtain DNA.

Facebook Twitter Pinterest Collecting blood for the DNA study from a wild cape parrot, Poicephalus robustus. The blood is collected by pricking a wing vein with a sterilised needle. Photograph: Colleen Downs/Willem Coetzer at al/PLoS ONE 2015

The team genotyped 138 individual parrots by sequencing a panel of 11 microsatellite loci. Microsatellites (microsats) are long tracts of non-coding repetitive DNA comprised of short tandem repeating sequences. Additionally, microsats are distributed throughout the genome of animals and are mutation hotspots.

Microsats analysis revealed Poicephalus form seven separate genetic clusters (Figure 2):

Facebook Twitter Pinterest Figure 2. The estimated population genetic structure of the Poicephalus species/subspecies used in the current study (K = 7). Each individual is represented by a vertical line, and coloured according to each individual’s estimated membership probability (Q-values). Average Q-values for each cluster is depicted above the figure. Illustration: Willem G. Coetzer et al./PLoS ONE 2015

These clusters correspond to the following species:



the red-fronted parrot, P. gulielmi (with P. g. gulielmi and P. g. massaicus clustering together; Q = 1; pink)



the brown-headed parrot, P. cryptoxanthus (pale blue)



Meyer’s parrot, P. meyeri (green)



Ruppell’s parrot, P. rueppelli (red)



This analysis also assigned the three Cape parrot subspecies to separate clusters:

the Cape parrot, P. r. robustus (dark blue)



the grey-headed parrot, P. r. suahelicus (yellow)



the brown-necked parrot, P. r. fuscicollis (purple), with only two P. r. fuscicollis individuals assigned to the P. r. suahelicus cluster with high probability (Q = 0.99)



“We were surprised to see that even though the Cape parrot (Poicephalus robustus robustus) and the grey-headed parrot (Poicephalus robustus suahelicus) co-occur in northern South Africa, they form two completely separate genetic clusters and we detected no recent exchange of genes between these two genetic clusters”, said co-author Sandi Willows-Munro, a senior lecturer in the genetics department at the University of KwaZulu-Natal.

“This is very strong evidence that the Cape Parrot forms a distinct genetic cluster separate from the other P. robustus subspecies and the other Poicephalus species”, said Dr Willows-Munro in email.

The team then asked whether and when any of these parrot populations were interbreeding by examining the genetic distance between Cape parrots (purple, yellow and dark blue dots, Figure 3) and five other Poicephalus species and subspecies. This analysis used pairwise comparisons of differences in microsatellite allele frequency using the fixation index, or F ST values (Figure 3):

Facebook Twitter Pinterest Figure 3. A 3D principal coordinate analysis (PCoA), generated in XLSTAT 2014. The pairwise FST values estimated between species/subspecies of the Poicephalus species included in the study were used to generate the figure. The first three axes explained 70.3% of the estimated variation. Illustration: Willem G. Coetzer et al./PLoS ONE 2015

The above figure shows a box that is a three dimensional representation of the calculated genetic distances between each of the Poicephalus taxa used in the study (Figure 3). Basically, the greater the calculated genetic distance between populations, the less interbreeding there is between them and the more spatially isolated they are from one another in the above figure, and vice versa.

“The genetic distance observed between the Cape Parrot and the other Poicephalus subspecies is again highlighted in this analysis”, said Dr Willows-Munro.

But what are the evolutionary relationships between the Poicephalus in this study? This simple question touches upon a complex ecological history. Since the Pliocene, southern Africa’s habitats have become increasingly fragmented due to increasing fire frequency and lack of rainfall. Further, the Quaternary global interglacial-glacial cycles drove the contraction and expansion of the forest biome in Africa. This contraction and expansion of forests is a major force driving speciation in many groups of forest-limited taxa in Africa.

“Speciation is a dynamic process. Recent work in Africa has highlighted several examples of rapid species radiations”, said Dr Willows-Munro. She also noted that habitat specialists, such as Cape parrots, may be particularly sensitive to habitat and climate change (doi:10.1016/j.ympev.2005.01.018).

Thus, it is no surprise that such rapid biome changes would drive rapid diversification in Poicephalus, too, which means their evolutionary relationships remain somewhat ambiguous.

To address this issue, the team reconstructed two phylogenetic trees. Phylogenetic analyses of concatenated DNA sequence data (left side; Figure 4), including mitochondrial markers, COI and 16S rRNA and the nuclear marker, β-fib, compared to mitochondrial gene tree (right side; Figure 4) confirmed that all Poicephalus species examined are monophyletic (they have just one ancestor) with the exception of the P. robustus clade (Figure 4):

Facebook Twitter Pinterest Figure 4. Maximum likelihood phylogeny retrieved of the Poicephalus specimens from the current study. The analyses were performed using (left) concatenated data (COI, 16S rRNA and β-fib) and (right) mitochondrial DNA data. Values given above the branches represent maximum likelihood bootstrap values and Bayesian posterior probabilities (in that order). Dated nodes are indicated by numbers next to each node in b). Species/subspecies were highlighted according to the microsatellite clustering analyses. Psittacus erithacus was used as an outgroup. Illustration: Willem G. Coetzer et al./PLoS ONE 2015

Although the phylogenetic gene tree reconstructed from the concatenated DNA analysis (left side, Figure 4) is poorly resolved for the P. robustus clade, the phylogenetic gene tree estimated from mitochondrial DNA (right side, Figure 4) is statistically well-supported; it shows that the three P. robustus forms do cluster together.

The team also conducted molecular clock analyses to identify when the three P. robustus forms diverged and found consistent estimates for the most recent common ancestor.

“The study of Coetzer et al. is quite challenging as they don’t even have fossils that can be used to calibrate their phylogeny, so they resorted to secondary calibrations from previous studies”, said evolutionary biologist Mario dos Reis, a lecturer at the School of Biological and Chemical Sciences at the University of London, who was not involved in this study.

“It is reassuring that estimates are relatively stable across the four analyses”, said Dr dos Reis in email.

These analyses estimated that the most recent common ancestor of the Poicephalus species included in this study is 10.27 to 10.63 million years ago (Mya). The origin of the Cape parrot clade is estimated at 6.16 to 6.72 Mya. Their data analysis places the most recent common ancestor between the Cape parrot and the two un-Cape forms, P. r. fuscicollis and P. r. suahelicus, at about 2 million years ago. Typically, separation of at least one million years is sufficient for speciation.

A young captive-bred un-Cape parrot . Photograph: Margaret Kemp-Adams

Dr dos Reis explained that these ages should not be interpreted as species divergence times, but rather as gene divergence times.

“These are really the coalescent times of the mitochondrial sequences rather than divergence times of P. robustus robustus subpopulations”, pointed out Dr dos Reis.



Basically, coalescent theory argues that different gene regions follow their own evolutionary pathways because of genetic recombination. These different evolutionary trajectories then give rise to different gene trees.

“Gene coalescent times can be substantially older than species divergence times”, explained Dr dos Reis. “For example, for the human-chimp divergence, genes coalesce about 6 Mya before the species divergence event, which we date at around 8 Mya.”

“Nonetheless the molecular phylogeny does suggest that P. robustus robustus forms a separate lineage from the other two subspecies, and thus I think conservation efforts to guarantee the survival of the subspecies are still worthwhile”, said Dr dos Reis.

All available evidence suggests Cape parrots are a real species

As you’ve probably realised, species concepts are slippery ideas. But the concept of what is a species is not only a scientific idea, but it is a conservation idea too. And conservation comes politics.

“Deciding what should and shouldn’t be considered a species is not a trivial exercise and many ways of making this decision have been proposed”, said conservation biologist Rowan Martin, manager for the World Parrot Trust’s Africa Conservation Programme and research associate at the Percy Fitzpatrick Institute of African Ornithology at the University of Cape Town, who was not part of this study.

“As the species is often considered the fundamental unit of conservation, the implications of this decision are also profound.”

A recent report based on 15 years of citizen science bird census data indicates there are less than 1600 wild Cape parrots remaining (doi:10.2989/00306525.2014.959088). But is this parrot a critically endangered species, as its numbers suggest? It depends upon whom you talk to. For example, the Cape parrot is considered to be “a distinct conservation unit” (a species) by the International Ornithologists’ Union and by BirdLife South Africa and for this reason, it is listed for protection in South Africa. It is also listed as “Endangered” in the Red Data Book of birds of South Africa, Lesotho and Swaziland. In contrast, the Cape parrot is listed as “Least Concern” in the IUCN Red List of Threatened Species because the Red List does not recognise the Cape parrot, P. r. robustus, as a species that is separate from the more widespread grey-headed parrot, P. r. suahelicus, and brown-necked parrot, P. r. fuscicollis. This controversy allows this endangered parrot species to fall through the cracks.

“Elevation of the Cape Parrot to full species level will lead to a reassessment of its threatened status on the IUCN and CITES species lists”, said Dr Willows-Munro. “Cape Parrots meet the criteria to be listed as Vulnerable in the IUCN Red List of Threatened Species, as well as all of the biological criteria for a CITES Appendix I listing.”

“Elevation to a species will also also increase public interest, as people tend to notice vulnerable and threatened species more than species of least concern”, said Dr Willows-Munro.

Facebook Twitter Pinterest A flock of wild cape parrots, Poicephalus robustus, flies overhead. Photograph: Colleen Downs/Willem Coetzer at al/PLoS ONE 2015

Wild Cape parrots face a variety of challenges to their continued survival, such as rampant habitat destruction -- mainly forest clearing for agriculture and logging of natural forests.

“Cape parrots once had a much more extensive range in South Africa, but following wide-spread clearance of Afromontane forests in the nineteenth and twentieth centuries they are now restricted to a mosaic of forest patches”, said Dr Martin in email.

Of course, Cape parrots are exploited in other ways, too.

“At the same time, they were also persecuted as a pest on pecan orchards and trapped in considerable numbers for the pet trade”, said Dr Martin in email. “A recent outbreak of Psittacine Beak and Feather Disease highlighted the vulnerability of remaining populations.”

Psittacine Beak and Feather Disease (PBFD) is an untreatable viral infection that is specific to parrots. Symptoms include a characteristic and irreversible loss of feathers and suppression of the immune system -- somewhat similar to HIV/AIDS in humans. This virus is transmitted by direct contact, typically from parents to their youngsters, and is almost invariably fatal in chicks and juvenile birds, although adult parrots may survive infection.

“Ironically, it was hoped that the [geographic] isolation of populations might afford protection from the spread of the disease but unfortunately this does not seem to be the case”, said Dr Martin. “The virus has been detected in all populations in which we have searched for it, suggesting the disease could be endemic to the Cape parrots in South Africa.”

Well, endemic or epidemic.

This study provides yet more evidence to the growing mountain of information that the Cape parrot is indeed, a distinct species. But to further nail this down, more work must be done: many more DNA markers from a wide variety of genomic loci must be analysed.

“[W]e are planning to do a more in depth phylogenetic study of the Poicephalus genus as a whole using additional nuclear DNA and mitochondrial DNA markers”, said Dr Willows-Munro.

“By reconstructing the evolutionary history of this genus we also hope to clarify the position of this new species within the genus and we will also better understand the factors driving speciation of this group in Africa”, said Dr Willows-Munro.

Source:

Willem G. Coetzer, Colleen T. Downs, Mike R. Perrin, Sandi Willows-Munro (2015). Molecular Systematics of the Cape Parrot (Poicephalus robustus): Implications for Taxonomy and Conservation, PLoS ONE 10(8): e0133376 | doi:10.1371/journal.pone.0133376 (OA)

also cited:

Jeffrey Rogers & Richard A. Gibbs (2014). Comparative primate genomics: emerging patterns of genome content and dynamics, Nature Reviews Genetics 15, 347–359 | doi:10.1038/nrg3707 (OA)

Mike R. Perrin (2005). A review of the taxonomic status and biology of the Cape Parrot Poicephalus robustus, with reference to the Brown-necked Parrot P. fuscicollis fuscicollis and the Grey-headed Parrot P. f. suahelicus, Ostrich: Journal of African Ornithology 76(3-4) 195-205 | doi:10.2989/00306520509485493 [£]

Sandi Willows-Munro, Terence J. Robinson, and Conrad A. Matthee (2005). Utility of nuclear DNA intron markers at lower taxonomic levels: phylogenetic resolution among nine Tragelaphus spp., Molecular Phylogenetics and Evolution 35(3) 624–636 | doi:10.1016/j.ympev.2005.01.018 [£]

Colleen T Downs, Morgan Pfeiffer and Lorinda A Hart (2014). Fifteen years of annual Cape Parrot Poicephalus robustus censuses: current population trends and conservation contributions, Ostrich: Journal of African Ornithology 85(3): 273–280 | doi:10.2989/00306525.2014.959088 [£]

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Erratum: This piece quoted the World Parrot Trust site as claiming there are only 1200 wild Cape parrots remaining. Their information is outdated. A 2014 report by Colleen Downs and colleagues states that “less than 1600 Cape parrots were recorded in the wild” (doi:10.2989/00306525.2014.959088). The piece was corrected at 0630 GMT on 13 August 2015 to reflect this newest census data.

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When she’s not reading or writing about parrots or interacting with them, GrrlScientist is tweeting about them on twitter @GrrlScientist.