Received Date : 16-Dec-2013

Accepted Article
Accepted Date : 27-Dec-2014

Article type : Review

Abundance and abundance change in the world’s

parrots

STUART J. MARSDEN* & KAY ROYLE

Division of Biology & Conservation Ecology, School of Science & the Environment, Manchester

Metropolitan University, Chester Street, Manchester M1 5GD, UK

Running head: Abundance and abundance change in parrots

* Corresponding author.

Email: s.marsden@mmu.ac.uk

This article has been accepted for publication and undergone full peer review but has not
been through the copyediting, typesetting, pagination and proofreading process, which may
lead to differences between this version and the Version of Record. Please cite this article as
doi: 10.1111/ibi.12236
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 Estimates of population density and abundance change (differences in density or
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encounter rates across land uses or time periods) form the cornerstone of much of our

knowledge of species’ responses to environmental conditions, extinction risks and

potential conservation actions. Gathering baseline data on abundance of the world’s c.

10 000 bird species and monitoring trends in the light of rapidly changing

environmental and harvest pressures is a daunting prospect. With this in mind, we

review literature on population densities and abundance changes across habitats in one

of the world’s largest and most threatened bird families, the parrots (Psittaciformes), in

order to identify gaps in knowledge, model phylogenetic and other influences on

abundance and seek patterns that might guide thinking for data-deficient taxa and

situations. Density estimates were found for only 25% of 355 parrot species.

Abundance change data were similarly limited and most came from logged forest, with

very few comparisons across different anthropogenic habitats. Threatened species were

no more likely to have a density estimate than non-threatened species, and were less

likely to have estimates of abundance change. Exploratory GLMMs indicated that

densities are most influenced by genus, and are generally higher within protected areas

than outside. It is unclear whether the latter effect stems from habitat protection, a

reduction in poaching, or both, but protected areas appear to be beneficial for parrots.

Individual members of the ‘parakeet’ genera (e.g. Pyrrhura and Eos) were predictably

abundant, while within larger-bodied genera such as Ara (macaws), species were

predictably uncommon (< 10 individuals per km2), and there was a long tail of extreme

rarity. Responses of parrots to habitat change were highly variable, with natural

variation in parrot abundance across different primary forests as great as that between

primary forest and human-altered forests. The speed at which environmental change is

affecting the world’s parrots far outstrips that of our current capacity to track their

abundance and we assess the likely scale of data deficiency in this and other bird

groups. Developments in survey and analysis methods such as variants of distance

sampling and the integration of niche modelling with point density estimation may

increase our effectiveness in monitoring parrots and other important and threatened

bird groups.

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 Keywords: conservation; distance sampling; Psittacidae; population density; habitat
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change.

Measures of population size, density and abundance change underpin much of our

understanding of the extinction risk that taxa or populations face (e.g. Collen et al.

2011), and contribute to the criteria on which the IUCN Red List extinction risk

classification system are based (Mace et al. 2008). While the quantitative data we are

able to gather on animal and plant abundance or abundance change are not without

problems (e.g. Wilson et al. 2011), they are often comparable across studies, species and

years by having an indication of precision (e.g. Bibby et al. 2000) and being open to

statistical testing (e.g. Maxwell & Jennings 2005), thus allowing more of the IUCN Red

List criteria to be assessed quantitatively. Reliable abundance measures can, however,

be difficult and costly to obtain for rare species of great conservation interest,

especially in remote or conflict-ridden regions (e.g. Buckland et al. 2008, Rovero &

Marshall 2009). There have been major developments in population estimation

recently, especially in approaches such as occupancy modelling, distance sampling and

mark-recapture/camera trapping methods (e.g. MacKenzie et al. 2006, Royle et al. 2009,

Thomas et al. 2010). Occupancy estimation, while not in itself yielding abundance

estimates, may require less effort than abundance estimation and, as such, can be

especially appropriate for rare species (MacKenzie et al. 2005).

Detecting changes in abundance requires counts or estimates of density or encounter

rate to be compared between time periods (longitudinal studies) or in cases where

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 space is substituted for time, whereby sites with different environmental conditions are
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sampled contemporaneously. Studies of the effects of land use on animals and plants

are more often done latitudinally (e.g. Gray et al. 2006), and thus involve an

assumption that treatment and control sites were identical before the land use change

occurred.

We review knowledge of population densities of one of the world’s largest but most

threatened bird families – the parrots - and assess how habitat and land use change

affect their abundance. First, we review the available data and identify where there are

important gaps in knowledge. Then we look for patterns in abundance and abundance

change to assess whether it is possible to predict the likely abundances of unstudied

species, based on information from those species for which there are data. Finally, we

compare our knowledge of parrots with that for other bird groups and assess prospects

for generating sufficient data for parrots and other birds to allow data availability to

keep reasonable pace with environmental change in the future.

The world’s parrots

Parrots are a group of approximately 350 mainly tropical and sub-tropical species,

occurring across much of the world, but with centres of high species richness in South

America (123 species), Central America/Caribbean (54 species), Australasia (108

species) and Asia (99 species; BirdLife International 2013;

www.birdlife.org/datazone/species accessed on 15 July 2014). In contrast, mainland

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 Africa has only 21 parrot species. Most species are birds of lowland forests or
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savannahs, although there are some highland forest specialists (e.g. Blue-eared Lory

Eos semilarvata) and a few species with unusual partial associations with grasslands

(e.g. Eastern Ground Parrot Pezoporus wallicus) or deserts (e.g. Princess Parrot Polytelis

alexandrae; Juniper & Parr 1998).

Parrots are well known to the general public as pets, exhibits in zoo collections,

and as flagships in conservation efforts (Verissimo et al. 2011), and they have a high

media profile. Some aspects of their behaviour are very well studied (e.g. Pepperberg

1999). Many parrot species, however, have not been the subject of dedicated ecological

study (Collar 1998, Masello & Quillfeldt 2002), and this lack of knowledge is a

particular concern given that parrots are disproportionately at risk of extinction

compared to other bird families (Bennett & Owens 1997). Forty-two per cent of the

world’s parrots are classified as ‘Threatened’ or ‘Near Threatened’ (BirdLife

International 2014; www.birdlife.org/datazone/species accessed on 15 July 2014),

largely due to habitat alteration and loss, and excessive capture for the pet trade

(Collar & Juniper 1992, Wright et al. 2001). Parrots have long been traded, and largely

uncontrolled capture for both the international bird trade (Pires 2012) and growing

domestic markets (Gastañaga et al. 2011) is a great cause for concern. Capture pressure

is, of course, uneven across years, taxa and geographical areas. Heavily traded groups

(from the CITES trade database www.unep-wcmc-apps.org/citestrade) include

Amazona spp (15 892 ‘wild-originated’ individuals for the five year period 2008-2012),

Ara spp (34 410 individuals), and Cacatua spp (15 694, most from Indonesia). Such

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 numbers are dwarfed by the colossal trade in the grey parrots Psittachus erithacus and
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P. timneh which involved over 140,000 wild-originated birds, many from Cameroon

and Democratic Republic of Congo, between 2008 and 2012 (www.unep-wcmc-

apps.org/citestrade).

METHODS

Data searching and coding

We searched for abundance data on all 356 extant parrot species currently recognised

by BirdLife International. We attempted to find all studies that reported either

estimates of population density (a quantification of the number of individuals within a

unit of area) or direct comparisons of density or encounter rate, between pristine/near

pristine habitats and one or more anthropogenic habitats/land uses, between two or

more pristine habitats (in different areas or across natural habitat types), or between

anthropogenic habitats. These data, which came from latitudinal, or, more rarely,

longitudinal studies (see above), formed the basis of our inferences about the responses

of parrot species to land use change. There is debate about the extent of pristine forests

(e.g. Willis et al. 2004) but here we consider the most pristine habitats available as being

the baseline against which to compare anthropogenic land uses.

We searched for published papers on Web of Knowledge (wok.mimas.ac.uk)

using combinations of key phrases (density, parrot, abundance, habitat change, land

use) and on the scientific name of every parrot genus and species. A few older studies

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 from books and grey literature were gleaned from an unpublished spreadsheet of
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population densities compiled for Birdlife International by Stuart Butchart (last edited

12 Nov 2002). We excluded density estimates from this source if they were based on

correspondence with no details of survey methods. However, most density estimates

were derived from distance sampling, for which field methods both for points and line

transects have been largely standardised since methodological work in the early 1990s

(Jones et al. 1995, Marsden 1999). We located unpublished PhD theses and unpublished

reports by searching the reference lists of relevant published papers, by searching the

BirdLife International library in Cambridge exhaustively, and by checking each

reference given in support of information on the species account for each parrot species

on BirdLife International’s Data Zone website. Finally, we searched manually through

around 2000 references held within the extensive parrot literature library of the

recently formed Parrot Researchers Group (parrot-specialist-

group@googlegroups.com). The full list of sources found is given in Supplementary

Online Appendix S1.

We did not include papers that compared parrot abundance between seasons but not

habitats (e.g. Renton 2002). We included studies that presented a single density

estimate, but not those that presented a single encounter rate from just one site/habitat

(e.g. Smyth et al. 2002). We sometimes had a choice between density estimates given in

a publication and, in such cases, we chose the estimate based on the largest sample

size. Studies of parrot populations outside their natural range (e.g. Rose-ringed

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 Parakeet Psittacula krameri in the UK; Pithon & Dytham 2002), intensively managed
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populations (e.g. Kakapo Strigops habroptila; Lloyd & Powlesland 1994) or research

study sites with experimental nest-augmentation (Cassagrande & Beissinger 1997)

were excluded.

The IUCN threat status of each species was recorded from BirdLife

International’s Data Zone, along with the region where the bulk of its natural range

currently occurs: Africa (AF) including Madagascar and Mauritius; Asia (AS);

Australasia (AU) including New Guinea, Australia, New Zealand, Fiji and the Pacific

islands; South America (SA) and Central America and the Caribbean (CA). The last two

regions were kept separate because, unlike SA, CA contains a number of small island

species, which are relatively well studied. The regions are also administered separately

within the Parrot Researchers Group. A few species ranged across more than one

region (mostly South and Central America, but also Australasia and Asia). These

species were assigned to the region in which the bulk of their range falls (from Juniper

& Parr 1998). Inevitably, there would be benefits to having a finer resolution to our

geographical categories, but small sample sizes (see later) meant that we were obliged

to work at a continental scale.

We recorded the following for each density estimate or abundance change:

species (following BirdLife International 2013); journal/document type and year of

publication; survey method used and whether the estimate was a density estimate or

an encounter rate. Survey methods were classified as line transect distance sampling

(DLT); point count distance sampling (DPC); line transect encounter rate (ERLT); point

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 count encounter rate (ERPC); spot-mapping (SM); roost counts (RC), and
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miscellaneous (MISC).

Population densities or encounter rates for non-forest/woodland parrot species (Kea

Nestor notabilis and Eastern Ground Parrot) were excluded from analyses except those

examining data availability. For forest/woodland species, abundance estimates within

each study were assigned to one of the following habitat categories according to

information given in those studies: primary (PR) including natural and little-disturbed

forest, woodland or savannah; selectively logged (SL) forests that had been recently

logged at an industrial-scale; secondary forest/woodland (SEC) that had regrown on

totally cleared land, or regrown in areas heavily altered in structure and floristics due

to small-scale logging and other forest uses; agricultural systems (AGR) including

small- and medium-scale systems (Scales & Marsden 2008); and plantation (PLAN)

including any scale of monocultural arboreal cultivation (e.g. Eucalyptus, coconut Cocos

nucifera, pine Pinus etc). Forest fragments (FRAG) were included if parrot abundance in

them was compared explicitly with abundance in non-fragmented forest, or with other

anthropogenic habitats.

Data analysis and modelling

Proportions of species with and without population density estimates were tested

across regions using a G-test, and across IUCN threat status (Threatened and Near-

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 threatened vs. Least Concern) using odds ratios and G-tests (including Yates’s
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correction). Abundance changes across pairs of habitat types (e.g. primary versus

selectively logged forests) were tested with Wilcoxon signed ranks tests as they were

paired within study. Absolute differences in abundance (differences in densities or

encounter rates not considering the direction of change) between primary forest and

each of the other habitat types (e.g. primary versus secondary tested against primary

versus agriculture) were examined using Mann-Whitney U-tests as they were not

paired by study.

We built exploratory generalised linear mixed models (GLMMs; Bolker et al.

2009) to identify, for forest/woodland species, likely predictors of density in primary

habitat. We regard this analysis as exploratory for several reasons (Zuur et al. 2010). We

had relatively few data points for the same species, and data were sparse compared

with the number of parameters we wished to include, so no interactions between

parameters were considered. We assumed a normal error distribution, and normalised

the dependent variable by converting it to its cube root.

Our predictors were genus, biogeographical region, survey method, and

whether or not the site was protected. Survey method was coded as one of the

following: DLT; DPC; and OTHMETH (other methods) which included spot mapping,

roost counts, long watches and other miscellaneous methods. Genera were included if

there were > 5 species cases within them - if not, they were included as OTHGEN

(other genera). A few closely-related genera were merged to increase sample sizes for

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 the analysis. Thus, Anodorhynchus, Primolius, Orthopsittacea, and Aratinga were merged
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with Ara (the macaws; Oliveira-Marques 2006), Calyptorhynchus was merged with

Cacatua, Charmosyna was merged with Trichoglossus, and Pionetes and Pyrilia were

merged with Pionus. Abundance estimates from primary habitat were coded as either

PROTECTED or NOT PROTECTED. The former included national parks and other

nature reserves, forest reserves or wildlife management areas, this information being

taken from the source publications.

We entered study as a random term to account for non-independence of

abundance estimates within studies. We combined a few studies (e.g. Riley 2002, 2003)

under the same study term if they used the same methods in nearby areas. Studies

reporting fewer than five density estimates were combined and included in the study

random terms as OTHSTUD (i.e. other studies). We used a random intercept model

(e.g. Zuur et al. 2009) as we were not so much interested in the intercept values of

‘study’ (a nuisance variable), as the likely contributions of predictors themselves.

Analysis was conducted within the package nmle in R (R Development Core Team

2013). We ranked models using minimisation of Akaike’s Information Criterion

corrected for low sample sizes (AICc) because of the relatively large number of

parameters per data point, and identified the variables most likely to appear in reliable

models by summing the Akaike weights of each model in which a variable appeared

(Symonds & Moussalli 2011). We present all models and AICc values in Appendix S2

andpresent confidence sets of ‘most likely’ models based on inspection of model

ranking scree plots.

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 RESULTS
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Data availability and quality

In total, we found 74 scientific papers, reports or theses containing density estimates or

abundance change data for parrots that fitted all our criteria for inclusion. Of these, 72

dealt with parrots in wooded habitats. Of 300 density estimates found, 253 (84%) were

derived using distance sampling, with 197 (66%) from point count distance sampling,

56 (19%) from distance line transects, and the remainder derived using spot-mapping

24 (8%) and a variety of other methods including nest or roost counting. Mean total

length of transects used for density estimates derived from distance-sampled line

transects was 676 ± 1001 km (SD; some surveys > 3000 km of effort; n = 48), and for

distance-sampled point count surveys was 190 ± 164 km (SD; n = 148). All density

estimates derived using distance sampling reported standard errors (SEs) or

confidence intervals. Density estimates derived from line transects had mean

coefficients of variation (CVs) of 31% ± 15 (SD; n = 41), while for point counts the mean

was 46% ± 23 (SD; n = 119).

At least one density estimate was available for 90 species (c. 25% of all 356

species). Most species had density estimates available from a single study but 22

species had estimates from two studies, 12 from three studies, and one species, Eclectus

Parrot Eclectus roratus, from five studies. The proportions of species with at least one

density estimate did not differ significantly across biogeographical region (G = 8.6, df =

4, P = 0.10), although Asia had a relatively high proportion of species with density

estimates (22 from 58) and Africa and related islands a relatively low proportion (two

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 from 24). Threatened species were no more likely to have a density estimate than non-
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threatened species (Odds ratio, non-threatened/threatened = 1.29; 95% CI = 0.78-2.15; G

= 0.76, df = 1, P = 0.38).

Density or encounter rate data that allowed comparisons of abundance across space or

time were available for 80 species (23% of all species) from 40 genera (Appendix S1).

Paired abundance estimates across habitat or across site were available for 179

habitat/site pairs. The most common comparisons were between primary forest and

selectively logged forest, and across different primary forest types/sites (Table 1). Most

comparisons were between primary forest and an anthropogenic habitat – there were

only 22 comparisons between different anthropogenic habitat types. Non-threatened

species were more likely to have a comparison of abundances across habitats than were

threatened species (Odds ratio, non-threatened/threatened = 3.13; 95% CI = 1.62-6.05; G

= 12.6, df = 1, P < 0.001).

Parrot population densities

Density estimates in primary forest/woodland habitats for those parrot genera with

more than eight density estimates are shown in Figure 1. Most Asian/Australasian

genera had higher estimated densities than those from the Neotropics – an exception

was the Asian genus Tanygnathus. Genera of larger-bodied parrots such as Ara,

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 Aratinga, and Tanygnathus had consistently low (< 10 individuals per km2) density
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estimates (Fig. 1). Abundances of species within five genera (Cacatua, Prioniturus,

Aratinga, Pionus and Amazona) were positively skewed – i.e. most species were rare but

there was a long tail of ‘commonness’ in a few species. Species with surprisingly high

abundances included Purple-bellied Lory Lorius hypoinochrous and the little-traded

Blue-eyed Cockatoo Cacatua ophthalmica of New Britain and the St Lucia Amazon

Amazona versicolor, one of the few island species in the Neotropical sample. In three

genera (Eos, Tanygnathus and Ara), abundances were negatively skewed, with most

species common but with a long tail of rarity.

Abundance change across habitats

Abundance changes from primary forest or woodland to anthropogenic habitats were

on average negative in all land uses except agriculture (Table 1). Paired tests of

abundance changes, however, pointed to significant differences only between primary

forest and secondary forest, between primary forest and plantation and, marginally,

between forest fragments and plantation. Importantly, abundance changes between

primary forest and secondary forest were modest compared to those of some other

land uses (e.g. absolute difference =1.70 as compared to 4.08 for selectively logged

forest), suggesting a consistent but not extreme decline in secondary forest as

compared with logged forest. Natural variation in parrot abundance across different

primary habitats was substantial and comparable with abundance changes between

primary and some anthropogenic land uses (Table 1)

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 Exploratory abundance/abundance change models
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The exploratory GLMM for abundance (density) estimates produced residuals that

appeared randomly distributed along the abundance axis. The distribution of residuals

in different genera appeared unremarkable but, as expected, was diverse for the group

OTHGEN. Genus appeared in almost all of the top models and had the highest Akaike

variable weight (Table 2; Appendix S2). Within the best supported model, coefficients

were significantly different from zero in six of eleven genera (OTHGEN excluded).

Protection was also a strong and significant candidate variable appearing in the top

three models and having an Akaike weight of 0.71. Densities tended to be higher in

protected areas. Choice of survey method made a negligible contribution to explaining

abundance variation.

DISCUSSION

How much do we know about abundance in parrots?

The lack of data is serious for all parrot groups, and acute for some, and we question

whether it will ever be possible able to gather enough data on parrots to inform

understanding of the effects of environmental change. Between 2000 and 2011, we

found density estimates for 68 species from 26 studies published or otherwise

available. Even if our extensive data trawl had detected only half of the estimates

actually available (a very conservative assumption) then the generation of density

estimates would still only be occurring at the rate of 12 species per year. If we then

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 assume that each species has an equal probability of being studied, then a density
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estimate will be generated for each parrot species approximately once every 30 years.

This is a serious degree of data deficiency when one compares this rate of data

generation to the timescales considered in Red List decline criteria or the periods over

which trade can escalate. For example, one Red List criterion is the percentage decline

over three generations, which is 9-48 years in parrots based on minimum and

maximum generation lengths given for parrot species in www.birdlife.org/datazone,

whilst exports of African Grey Parrot Psittacus erithacus increased from under 18 000 in

1997 to over 42 000 in just two years (www.cites.org/eng/resources/trade.shtml). Lack

of knowledge of spatial variation in species’ abundance may be even more severe.

Scarlet Macaw Ara macao has an extent of occurrence well in excess of 5 million km2

and has just four density estimates from a single study (Lee & Marsden 2012). There is

likely to be great variation in abundance across a species’ range, for example between

densities at the periphery of its range compared to that in the centre (e.g. Gaston et al.

1997). There are big differences in parrot abundance across discrete geographical units

such as islands (e.g. Lambert 1993, Marsden 1999). Eclectus Parrot is the best studied

species, with estimates from five studies, but it occurs on over 50 islands across its

range (Juniper & Parr 1998).

In terms of volume of conservation research output (number of conservation-

oriented scientific papers per species), the Psittaciformes are unremarkable, being

ranked 13th of 25 bird orders by Brito and Oprea (2009). Our findings, in terms of

availability of abundance estimates for parrots, resonate with the findings of de Lima et

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 al. (2011), who reported that over half of the world’s ‘restricted range’ island bird
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species had not been the subject of published study. Particularly worrying was that

Globally Threatened species were no more likely to have a density estimate than non-

threatened species, and were less likely to have a comparison of abundance changes

across habitats. Generally, threatened bird species are no more the focus of scientific

research than are non-threatened species (Brooks et al. 2008). Of course, there are also

situations where studies of threatened parrots have gone beyond abundance

estimation to demography (Beissinger et al. 2008) or intensive management (e.g.

Houston et al. 2007), but such cases are not the norm across the order. With such huge

data gaps and with no evidence for any recent increase in research output (98 density

estimates were published during the 1990s, and 66 from the period 2000-2009), there

seems to be insufficient capacity to track abundance of parrot species in response to

environmental changes.

Patterns in abundance and abundance changes

In some genera, we can be reasonably sure of approximate density estimates for most

species in pristine habitats. For example, Tanygnathus, Aratinga and Ara appear to

comprise invariably low density species. In other groups, such as Pionus, Cacatua and

Amazona, densities of 10 per km2 are the norm, but there are individual taxa or

situations in which species can achieve unusually high densities. In the case of these

taxa, it was species such as Purple-bellied Lory, Blue-eyed Cockatoo and St Lucia

Amazon that were particularly common. All of these species occur on islands, but

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 perhaps more importantly, the first two are little-traded species (Marsden & Pilgrim
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2003), while the third is the subject of successful conservation action (e.g. Collar 1997).

In a conservation context, errors arising from assuming rarity but finding abundance

are not a great problem. However, there appear to be other genera (e.g. Eos, Lorius)

within which most species in most situations are common but a few are unusually rare.

This is a bigger problem for conservationists dealing with unstudied species, as it

means we may overlook species with very low populations. Examples include the

order of magnitude difference in the densities of Chattering Lory Lorius garrulus in

North Maluku (Lambert 1993) compared to this and other Lorius species elsewhere (e.g.

Poulsen 1998; Marsden & Pilgrim 2003).

Models suggested that parrot abundance in primary habitat was most strongly

linked to two predictors - genus and forest protection. The former again lends weight

to the idea that there is a phylogenetic signature in parrot abundance, as has been

found in other taxonomic groups (e.g. Kelly et al. 2008). There has been much recent

attention to the effectiveness of protected areas for biodiversity conservation (e.g.

Andam et al. 2008, Rayner et al. 2014). Protection, including national park status and

other designations, does not always provide strict protection to either parrots or the

forest in which they live (e.g. Metzger et al. 2010), so it is encouraging that protection

was an important predictor of higher parrot densities. How much of this is due to

maintenance of forest quality generally (e.g. Nepstad et al. 2006) or protection of

specific resources such as nest holes (e.g. Gibbons & Lindenmayer 1996), or how much

is a result of reducing direct exploitation (Wright et al. 2001) is unknown.

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 A lack of data, and the great diversity of land use changes occurring within the
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ranges of most parrots, coupled with complications of bird capture and other

environmental changes, meant that we had little power to predict species’ responses to

habitat alterations. Responses to conversion of primary forest to, for example,

secondary forest or through logging were highly variable but tended to be negative.

An exception was conversion to small-scale agriculture, which if anything, benefited

more species than it negatively affected. As with the other across-habitat abundance

comparisons, we could not gauge the importance of small-scale agriculture in

supporting threatened parrot species in particular simply because so few threatened

species were included in the analysis due to a lack of data. Studies of parrots in small-

scale agriculture have found high food availability in this habitat as compared with

primary forest (Marsden & Pilgrim 2003) and a high usage by frugivores of agricultural

plots which border more pristine forests (Marsden & Symes 2008). The variation in

parrot responses to land use change mirrors the diversity of abundance changes noted

within some taxa across land uses found by others (Gray et al. 2007, Scales & Marsden

2008). Many Red List classifications are built on assumptions that a taxon will react to a

given land use change at an unstudied site in a certain way based on reactions of the

same or related species elsewhere or to a different land use change. Clearly, further

work to make sense of the responses of parrots and other groups to land use changes,

and especially comparisons across anthropogenic land uses (e.g. monocultural

plantations vs. small-scale agroforests) could yield enormous benefits, if clear patterns

can be found.

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 Survey methods and methods development
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Distance sampling methods have become preferred for estimating population densities

of parrots, and indeed many other families of birds (Buckland et al. 2008). While not

always well suited to tropical conditions and parrots, we suggest that they remain the

best option for parrot ecologists outside situations in which total counts can be made,

or perhaps where roost counts are feasible (e.g. Matuzak & Brightsmith 2007). There

have also been recent advances in tailoring distance sampling methods to individual

situations such as tall, structurally complex Amazonian forests, through the use of a

cue-counting variant of line transects (Lee & Marsden 2012). Recent work has also

produced a calibration by which ‘ball-park’ population densities of the heavily-traded

African grey parrots can be estimated from simpler encounter rates (CITES 2013).

Importantly, choice of survey method (distance line transects, distance point counts

and ‘other’ including roost counts) did not have a consistent influence on parrot

density estimates. This is reassuring for two reasons. First, point counts have

sometimes been found to inflate bird densities over those of line transect and other

methods (e.g. Casagrande & Beissinger 1997). Second, several reference works suggest

the use of line transects rather than point counts where the target species is likely to be

rarely encountered (e.g. Bibby et al. 2000; Buckland et al. 2008). This may mean that

survey method choice is something of a self-fulfilling prophecy, tending to make

transect-derived estimates lower than point count estimates. We found no evidence of

an effect of method choice, and while we caution that some method-related influence

might be associated with regional or taxon-related bias in method choice, we can report

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 that the influence of method on parrot density estimates does not appear to be
Accepted Article
unworkably great.

Population studies of many threatened parrots and other birds are frustrated by

low population densities, which make accumulation of sufficient records for reliable

abundance estimation very time- and resource-consuming (Marsden 1999). There is, of

course, no easy solution to this problem, but there are procedures that can allow

distance sampling to be used reasonably effectively with rare species. Espanola et al.

(2013) combined the 63 records of four rare parrots (genera Tanygnathus and

Prioniturus) from forests on Luzon, Philippines, to estimate a common detection

probability and derived species-specific density estimates, including those for rare

species, using the multiplier function in DISTANCE. A variant of this procedure would

either enter species as a covariate in DISTANCE, or use the detectability characteristics

of species (body size, call rate, behaviour, stratum used) to pair up species and use the

many records of the more common species to model detection in the rarer one (with

the assumption that detectability is indeed equivalent; Buckland et al. 2008). With the

above procedures, we believe it is possible to derive useful, if imprecise, density

estimates with as few as ten records of the target species.

Finally, presence-only species distribution models (SDMs) such as MAXENT

are being increasingly used to predict ranges and range changes (e.g. Marin-Togo et al.

2012), and examine habitat suitability and likely areas for reintroduction (Thorn et al.

2009). While not useful per se for abundance measurement, they can feed into other

criteria for Red List assessment, specifically extent-of-occurrence and area-of-

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 occupancy metrics (Mace et al. 2008). However, recent work has found a workably
Accepted Article
strong link between probability of occurrence at locations, derived from SDMs, with

corresponding point estimates of density from field surveys (e.g. van der Wal et al.

2009). There are issues to overcome, particularly with rare species with few or highly

clustered location data, and with predicting accurately actual local density rather than

maximum potential density (Torres et al. 2012), but the methods show promise. If a

workable relationship between occurrence probability and local density is found for

parrots, then coupling the two methods, while not negating the need for field surveys,

may greatly increase our ability to predict abundance and abundance changes for a

fuller range of parrot species across huge areas.

Our thanks go to those authors who kindly shared copies of their published papers

with us, and to Carlos de Araújo and Juan Masello for making the virtual library of the

Parrot Researchers Group available to us. Thanks also to BirdLife International in

general, and Stuart Butchart in particular, for making available to us their database of

bird population densities.

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 Table 1. Directional and absolute (sign disregarded) proportional differences (mean ± 1
Accepted Article SD) between abundance estimates in different habitats (including different types of
primary forest). Values of 1.0 indicate identical abundance in the two habitats; 1.50
indicates a difference of 50%. In brackets are the numbers of species whose abundance
declined to zero. Also shown are the number of species with pairwise comparisons and
the significance of a Wilcoxon signed ranks tests (including species that declined to
zero). PR = primary/disturbed primary forest; SL = selectively logged; SEC = secondary;
AGR = small-scale agriculture; PLAN = monocultural arboreal plantation; FRAG =
forest fragment. Below the figures for absolute differences are significant pairwise
differences: * P < 0.05; ** P < 0.005; ns not significant.

PR SL SEC AGR
PLAN FRAG

Directional changes

PR -1.43 ± 6.2 (3) -0.91 ± 1.7 (1) +0.78 ± 3.8 (2)

-2.04 ± 1.1 (9) -1.48 ± 8.6 (3)

n= 31 n = 47 ns n = 24 ** n = 21 ns
n = 12 ** n = 18 ns

SL n=0 n=3
n=0 n=0

SEC -0.38 ± 2.0 (0)

n = 9 ns
n=2 n=0

AGR
n=2 n=0

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 PLAN
Accepted Article + (6)

n=6*

Absolute differences

PR SL SEC AGR
PLAN FRAG

PR 3.02 ± 3.93 4.08 ± 4.87 1.70 ± 0.84 3.05 ± 2.33

2.04 ± 1.07 4.23 ± 7.51

SEC** SEC**, AGR* SEC*

Table 2. Confidence sets for exploratory GLMMs explaining parrot abundance in

primary forests. Five models are shown (an asterisk denotes the variables included)
with the sixth having a ∆AICc of 5.39. Also shown in bold are Akaike variable weights.
Coefficients ± standard errors are shown for the ‘best’ model. ‘Prot’ indicates whether
or not the study site was officially protected area (see text for details). ‘Method’ refers
to survey method used count parrots. All models are shown in Appendix S2.

Abundance

Genus Region Prot Method ∆AICc

0.86 0.67 0.71 0.03

* * * 0

* * 0.01*

* * 1.55

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 * * 2.11
Accepted Article
* 2.92

Coefficients from most competitive model (marked * above)

Coeff ± SE

Ara -0.340 0.180

Brotogeris +0.184 0.246

Cacatua +0.659 0.229

Eclectus +0.199 0.292

Eos +1.149 0.263

Loriculus +1.019 0.324

Lorius +0.960 0.254

Pionus -0.120 0.184

Prioniturus +1.189 0.282

Pyrrhura +0.174 0.238

Trichoglossus +1.017 0.326

OTH genera +0.592 0.184

Protected (Yes) +0.317 0.111

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 Figure 1. Boxplots of densities in primary forest for individual species within eleven
Accepted Article data-rich and larger parrot genera. Only forest/woodland species are included. Shown
are the median, upper and lower quartile (within box), upper and lower quartile plus
1.5 x interquartile range (bar) and outliers.

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