Research Article |
Corresponding author: Denis A. Saunders ( carnabys@hotmail.com ) Academic editor: Klaus Henle
© 2018 Denis A. Saunders, Nicole E. White, Rick Dawson, Peter R. M. Mawson.
This is an open access article distributed under the terms of the Creative Commons Attribution License (CC BY 4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
Citation:
Saunders DA, White NE, Dawson R, Mawson PRM (2018) Breeding site fidelity, and breeding pair infidelity in the endangered Carnaby’s Cockatoo Calyptorhynchus latirostris. Nature Conservation 27: 59-74. https://doi.org/10.3897/natureconservation.27.27243
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The ecology and behaviour of the endangered Carnaby’s Cockatoo Calyptorhynchus latirostris have been studied in detail at Coomallo Creek in the northern wheatbelt of Western Australia from 1969 until the present. Results of research on this breeding population conducted on individually marked birds from 1970 to 1990 were compared with results from analyses of DNA taken from nestlings in the study area from 2003, 2005, and each year from 2009 to 2013. Analyses of DNA confirmed earlier findings about the stability of adult breeding pairs, and that females used the same breeding hollow they used previously, provided the hollow was not occupied when they returned to breed. When moving to another hollow, they chose a hollow in the same vicinity of the previous hollow. Analyses in 22 cases where DNA was obtained from both nestlings of a breeding attempt revealed that in six (27.3%) cases, the second egg was fertilised by a male not paired with the female. These extra-pair copulations were not suspected during the earlier study based on observations of individually marked birds.
Carnaby’s Cockatoo, Calyptorhynchus latirostris , nestling DNA, extra-pair copulations, pair bond stability, nest site fidelity
Carnaby’s Cockatoo Calyptorhynchus latirostris is endemic to south-western Australia. Formally common throughout its range, over the second half of the last century, extensive clearing of native vegetation for the development of broadscale agriculture and urban development saw the species contract significantly in range and abundance. As a result of the loss of breeding and foraging habitat (Fig.
Location of Coomallo Creek study area, and distribution of Carnaby’s Cockatoo (between the coast and the black line). Carnaby’s Cockatoo has significantly decreased in range and abundance as a result of loss of breeding and foraging habitat. The extent of the loss of habitat (native vegetation indicated in pale yellow) is illustrated clearly in this satellite image.
Beginning in 1968 and continuing, the ecology and behaviour of the species has been the focus of one of the longest running vertebrate studies in Australia (
The fact that Carnaby’s Cockatoo is rare, and difficult to breed in captivity (
In this paper we examine the use of DNA taken from nestlings of one breeding population over seven breeding seasons (2003, 2005, 2009-2013) to investigate aspects of the breeding biology of Carnaby’s Cockatoo. We compare the results obtained from DNA analyses with earlier research (1969-1996) on the population using observations of individually marked birds to test the efficacy of analyses of nestling DNA for studies of breeding behaviour.
The Coomallo Creek (Fig.
From 1969 to 1996 the area was visited for 21 of those years for at least one week in early September, and one week in early November. During each visit every known nest hollow was inspected, and the identity of breeding females established if possible by trapping or by using a telescope to read the number on the bird’s leg band/ring. Both methods were time consuming, and it was not possible to identify all banded females. Searches were also undertaken to find any nesting hollows in use not registered in the study area. Any nestlings older than three weeks were measured (length of the folded left wing and body mass) and banded with a stainless steel band with a unique number. Nestlings were aged using the methods of
The area was visited once in November 2003 and 2005, and each year from 2009 to 2013 the area was visited for one week in early September and early November, with a three-day visit in early January to establish nesting success, and band any nestlings laid late in the season. The identity of breeding females was established by photographing their legs, and checking for bands using the methods of
Material taken for DNA analysis was plucked with tweezers or cut with scissors, and placed in a vial of preservative (20% dimethylsulphoxide saturated with sodium chloride). The vial was labelled with species identification, collection date, name of collector, name of the study area, nest hollow number, and the description of material taken (e.g., 4 feathers, small dead nestling, toe of dead nestling). All equipment used for handling DNA was washed in disinfectant, 90% ethanol, and rinsed with water between samples to ensure no cross-contamination of DNA.
A total of 309 DNA samples were collected from Coomallo Creek between November 2003 and October 2013 for DNA extraction with Qiagen Blood and tissue kit (Qiagen). Samples were subjected to a real-time quantitative PCR (qPCR) assay to assess the DNA extracts for quality and quantity of nuclear DNA prior to microsatellite genotyping. Genetic profiles were generated from 16 microsatellite markers as previously published by
The software COANCESTRY 1.0.1.7 (
Distances between nest hollows used successively by the same breeding pair were calculated using the “show distance between waypoints” function of OziExplorer® software. The density of nest hollows in the study area was only calculated for the period 1972-1990 and 2009-2013 due to the fact that nest hollows were being located for the first time at a high rate during the first two years of the study (1970–1971).
Between 1970 and 1990, observations of individually marked females provided data on nest hollow use by 92 breeding pairs, each making two or more breeding attempts. Pairs recorded making two or three breeding attempts provided 68.5% of the data. During that period one female was recorded making 12 breeding attempts (Table
Number of breeding attempts made by individual females 1970–1990 and 2009–2013.
Number of breeding attempts made by individual females | 2 | 3 | 4 | 5 | 6 | 7 | 8 | 9 | 10 | 11 | 12 | Total |
---|---|---|---|---|---|---|---|---|---|---|---|---|
1970–90 | 45 | 18 | 15 | 7 | 2 | 1 | 1 | 0 | 2 | 0 | 1 | 92 |
2009–13 | 24 | 11 | 4 | 2 | 1 | 0 | 0 | 0 | 0 | 0 | 0 | 42 |
Data were obtained from 172 successive breeding attempts from the 92 pairs between 1970 and 1990, and 63 successive breeding attempts from 42 pairs between 2009 and 2013 (Table
The breeding outcome from, and location of, successive hollows used for breeding by 92 females 1970–1990 and 34 females 2009–2013. Figures in brackets are percentage of the total.
# individuals | Successful; same hollow | Successful; different hollow; previous hollow occupied or unusable | Successful; different hollow; no information on hollow use | Unsuccessful; same hollow | Unsuccessful; different hollow | Total | |
---|---|---|---|---|---|---|---|
1970–90 | 92 | 77 (45) | 56 (33) | 9 (5) | 2 (1) | 28 (16) | 172 |
2009–13 | 34 | 28 (44) | 23 (37) | 4 (6) | 1 (2) | 7 (11) | 63 |
During the period 1970-1990, data on movements to different hollows between successive breeding attempts were obtained from 60 females that moved 94 times, and 2009-2013 from 30 females that moved 40 times (Fig.
Movements between successive hollows by four females (two banded and two unbanded), confirmed by analysis of nestling DNA; a female 210-01694 fledged from T116 in 1990, and nested successfully each year from 2009 to 2012 in the hollows indicated b female 210-01876 was banded as an adult, and she nested successfully from 2009 to 2012 in the hollows indicated c unbanded Female A nested successfully in T43 from 2009 to 2012, was unsuccessful in T43 in her first breeding attempt in 2013, moved to CWB304 in which she was successful in her second breeding attempt that year d unbanded Female B nested successfully from 2009 to 2012 in the hollows indicated. The scale is indicated in the white rectangle with the width of the rectangle indicating the distance.
Mean distance (km) between nest hollows used by Carnaby’s Cockatoo in successive breeding attempts 1970–1990 and 2009–2013.
Years | Mean±s.d. distance moved (km) | Median distance moved (km) | Range | # individuals | # movements |
---|---|---|---|---|---|
1970–1990 | 0.66±0.74 | 0.36 | 0.02–4.05 | 60 | 94 |
2009–2013 | 1.25±1.31 | 0.56 | 0.07–5.50 | 30 | 40 |
Density of nest hollows (km-2) used by Carnaby ’s Cockatoos 1972–1990 and 2009–2013.
Years | Mean±s.d. density of nest hollows (km-2) | Range |
---|---|---|
1972–1990 | 14.0±4.9 | 4.5–23.8 |
2009–2013 | 16.9±4.8 | 11.2–23.8 |
For the period 2009-2013, DNA was obtained from both nestlings from 22 breeding attempts. Of these, six (27.3%) of the sibling pairs had different males fertilising the two eggs. Both nestlings fledged successfully in 13 cases where both eggs were fertilised by the same male (13/16 = 81.3%), and in four cases where the eggs were fertilised by different males (4/6 = 66.7%). Of the five cases where one or both of the nestlings died, both eggs were fertilised by the same male in three (60%) cases, and two (40%) by different males. The ages of three of the adult females for which there were DNA data on both nestlings from a single breeding attempt were known as the females were banded. Band number 210-03089 was at least 22 (she was banded as an adult), and both eggs were fertilised by the same male; 210-01876 was at least 26, 27 and 28, and the same male fertilised both eggs in all three clutches; and 210-01694 was 20, and the two eggs were fertilised by different males.
The average time between the laying of the two eggs in each case of siblings for which laying dates were known was 10.6±3.9 days (n = 15; range 5-17 days) where the same male fertilised both eggs, compared with 14.8±5.9 days (n = 5; range 9-24 days) where the second egg was fertilised by a different male. There was no significant difference in the mean interval (in days) between the laying of successive eggs in nests fathered by the same male and different males (t-test: t=-1.71, d.f.=17, p=0.053).
Nest site fidelity, breeding site tenacity or breeding philopatry is a well-known phenomenon, demonstrated by many vertebrate species (
Carnaby’s Cockatoo breeds in highly stable habitats (sensu McNicholl), in that tree hollows are usually available for many years (
The chances of observing extra-pair copulations of individually marked birds were low. While many breeding females were individually marked with patagial tags and/or leg bands, far fewer males were individually marked. While copulations were observed, those few cases where both sexes were identified were all with known mates, reinforcing the conclusion of monogamy. In 2010 a documentary about the breeding of Carnaby’s Cockatoo was filmed (http://www.abc.net.au/tv/guide/abc1/201203/programs/NH1001W001D2012-03-13T203229.htm accessed 5 April 2018). The documentary was based on one breeding pair, and after the first egg was laid, film was taken of the female leaving the hollow when her unbanded mate was not around. There were two adult males nearby, and both immediately started courtship displays towards the female. One of the males had a leg band, and that could have only been placed on the bird seven years previously or longer. Earlier observations and this film clearly indicate that males will readily court breeding females other than their mates (
Who were the males responsible for these extra-pair copulations? Of the six cases known to us, in three cases, there were no data indicating the second nestling was a half-sibling to any other nestlings from the area that breeding season for whom we had DNA. In each of the other three cases (one in 2009, 2010 and 2012), there was a nestling from three other breeding pairs that indicated a half-sibling relationship. The average distance between any of these hollows and the hollow with the extra-pair copulations was 2.8±1.2km (range 1.7–5.2km). If it was one of the males producing the half-siblings, they weren’t neighbours. Without DNA from the males, unfortunately we cannot identify any of the males responsible.
The conservation implications for such extra-pair fertilizations in Carnaby’s Cockatoo are difficult to discern. Extra-pair fertilizations within local breeding populations would result in broader genetic diversity within breeding populations than would result from purely monogamous pairings.
Comparisons of results obtained from long-term studies based observations of individually marked Carnaby’s Cockatoo breeding adults, and those from analyses of DNA from Carnaby’s Cockatoo nestlings showed that analyses of DNA are useful for establishing stability of breeding pairs and breeding site fidelity. Analyses of nestling DNA demonstrated that aspects of mating behaviour that would be extremely difficult to show using observations of individually marked adults could be revealed by studies of DNA. Analyses of DNA from nestlings over subsequent breeding seasons would be necessary to investigate the identity and ages of the adults involved in extra-pair copulations, and provide evidence of the advantages to the species of breeding pair infidelity.
The field work and animal handling reported here were conducted under appropriate ethics approvals (held by CSIRO staff for the period 1970-1990, and Western Australian Department of Biodiversity, Conservation and Attractions Animal Ethics Committee project approval numbers 2011/30 and 2014/23 for the later period) and bird banding approvals [Australian Bird and Bat Banding Authority #418 held by DAS (1970–1990), and #1862 held by PRM (2003-2013)]. We are grateful to the following for assistance: the Raffan, Paish, McAlpine and Hayes families who supported field work on their properties; the Raffan family who provided accommodation during field work in the area; Palm Beach Rotary Club, and in particular Mr Desmond Mant and Mr Alan Guthrie for their tireless assistance with installing/repairing and monitoring hollows in the field; Dr Manda Page for support; Ms Amy Mutton who prepared Fig.