Egg-laying and rainfall synchrony in an endangered bird species: Implications for conservation in a changing climate

Biological Conservation 161 (2013) 1–9

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Egg-laying and rainfall synchrony in an endangered bird species: Implications for conservation in a changing climate Denis A. Saunders a,⇑, Brendan A. Wintle b, Peter R. Mawson c, Rick Dawson d a

CSIRO Ecosystem Sciences, GPO Box 1700, Canberra, ACT 2601, Australia School of Botany, University of Melbourne, VIC 3010, Australia c Perth Zoo, 20 Labouchere Road, South Perth, WA, Australia d Department of Environment and Conservation, Locked Bag 104, Bentley DC, WA 6983, Australia b

a r t i c l e

i n f o

Article history: Received 5 December 2012 Received in revised form 29 January 2013 Accepted 6 February 2013

Keywords: Carnaby’s Cockatoo Calyptorhynchus latirostris Breeding seasons Synchrony between rainfall and egg-laying Climate change

a b s t r a c t Birds use a number of environmental cues to time their breeding season to maximise their chances of raising young when food is most abundant. Such cues include photoperiod, temperature and rainfall. In very arid regions, birds may start egg-laying with the onset of rain to allow fledging to coincide with the availability of grass seeds. However the influence of rainfall on timing of egg-laying in areas with variable, but more reliable, rainfall has not been as clear. Carnaby’s Cockatoo, an endemic species of southwestern Australia, a region with a Mediterranean climate, is known colloquially as ‘‘the rainbird’’ as its movements to the breeding areas appear to coincide with the start of the wetter part of the year. Here we use a long-term data set on the breeding of this species (24 years of data from 1969 to 2011) to quantify the link between the timing of autumn rains and the commencement of egg-laying in this endangered cockatoo. We found a tight synchrony which indicates a strong reliance of the species on early autumn rains as a cue for breeding. We describe the conservation implications of increased variability in timing and quantity of rainfall for the long-term viability of Carnaby’s Cockatoo. Ó 2013 Elsevier Ltd. All rights reserved.

1. Introduction Lack (1954) and others (Visser et al., 2004; see review by Dawson, 2008), have pointed out that there is great selection pressure on birds (and other animals) to make sure they time their egg-laying (and the sizes of their clutches) to maximise the chances of reproductive success. That is, they time the production of their offspring to coincide with the time of year when food resources are most abundant. The cues they use to begin egg-laying should provide them with information about when food will be plentiful when raising young later in the breeding season when energetic demands are highest. There have been many studies on environmental cues for timing of egg-laying in birds. A number of cues (photoperiod, temperature, food availability and rainfall) have been found to be relevant to individual species and in some cases these may act in synergy (Dawson, 2008). At any latitude, changes in photoperiod within and between years are predictable and have been found to be a fundamental cue to time breeding, moult and migration (Dawson, 2008), particularly in birds in regions such as North America, Asia ⇑ Corresponding author. Tel.: +61 2 6255 1016. E-mail addresses: [email protected] (D.A. Saunders), b.wintle@ unimelb.edu.au (B.A. Wintle), [email protected] (P.R. Mawson), [email protected] (R. Dawson). 0006-3207/$ - see front matter Ó 2013 Elsevier Ltd. All rights reserved. http://dx.doi.org/10.1016/j.biocon.2013.02.004

and Europe, with defined seasonality and predictable availability of food (Astheimer and Buttemer, 2002; Dawson, 2008). Species with regular breeding seasons may also use photoperiod cues, together with ambient temperature to vary timing of breeding from year to year (Visser et al., 2004). While much research attention has been paid to the role of photoperiod, other environmental cues have been found to influence timing of breeding. For example, species in arid regions, that breed irregularly, may opportunistically use increases in food availability as a result of rainfall (e.g., Zebra Finch Taeniopygias guttata Immelmann, 1973; Zann et al., 1995; Zann, 1999), or some other weather phenomena (e.g., Banded Stilt Cladorhynchus leucocephalus Saunders and de Rebeira, 1986). Spotted Antbirds Hylophylax n. naevioides, a neo-tropical rainforest species, exhibited seasonality of reproduction with variation in commencement of breeding in a region with limited changes in photoperiod (Wikelski et al., 2000). Wikelski et al. (2000) hypothesised that the birds anticipated rainforest seasonality using tropical photoperiod as a long-term cue and fine-tuned breeding using food availability and/or rainfall as short-term cues. In southwestern Australia, with its semi-arid, Mediterranean climate of hot, dry summers and cool, wet winters, many bird species breed in the Austral spring (Serventy and Whittell, 1976; Halse and Jaensch, 1989), that is, in the warm season between the cool, wet winter and the hot, to very hot, dry summer. However, there

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are no studies of which we are aware on the influence of rainfall on the timing of egg-laying of any species of bird in this region. Carnaby’s Cockatoo Calyptorhynchus latirostris is endemic to southwestern Australia. It breeds in the Austral winter and spring with egg-laying taking place between July and November (Saunders, 1982). The biology of Carnaby’s Cockatoo is apparently linked to seasonal weather patterns. For example, its movements with the onset of rains from the areas along the coast where it spends the hot, dry, non-breeding season (January–June) to the inland areas where it breeds in the cooler, wetter period of the year, resulted in the species being known to Noongyar people (the region’s Aboriginal people) and to European settlers as ‘‘the rainbird’’ or as ‘‘harbingers of rain’’ (Serventy and Whittell, 1976). While the biology of the species has been extensively studied (Saunders, 1982; Saunders and Ingram, 1998), there has, to date, been no direct analysis of its dependence on rainfall as a cue for migration and breeding. Recent concern about the implications of decreasing total rainfall and increasing rainfall variability between years (CSIRO, 2007) prompted a quantitative analysis of the link between rainfall and breeding. The results of this analysis may have significant conservation implications for a wide range of species that are reliant on timing of rainfall as a cue to commence breeding. Consequently, the aims of this paper are to: 1. investigate the timing of the commencement of egg-laying in Carnaby’s Cockatoo in relation to seasonal rainfall; 2. establish if individual females, over a series of seasons, commence egg-laying each season at the same time in relation to the first egg laid by the species that season; and

3. discuss the conservation implications for the species under a changing climate. 2. Materials and methods 2.1. Climate of the southwestern Australia Southwestern Australia has a Mediterranean climate of hot, dry summers and cool, wet winters. Average annual rainfall varies from around 300 mm at the drier extent of the range of Carnaby’s Cockatoo to more than 800 mm at Busselton in the far southwest of Western Australia (Fig. 1). Less than 18% of annual average rainfall occurs between October and March (mid-spring to early autumn) and more than 38% falls in June and July (winter). January and February are the hottest months (average maximum 34.7 °C and minimum 17.7 °C) and July is the coolest (17.6 °C and 7.2 °C) (all data for Badgingarra Research Station (30°340 S; 115°540 E) with a 50 year average sourced from Australian Bureau of Meteorology (http://www.bom.gov.au/climate/averages/tables/ cw_009037.shtml, accessed 25 September 2012). 2.2. Carnaby’s Cockatoo Carnaby’s Cockatoo has been extensively studied (Saunders and Ingram, 1998 and references therein). By the 1980s the species had undergone a major reduction in range and abundance as a result of extensive clearing of native vegetation for the development of broadscale agriculture. This decline has been well-documented (Saunders and Ingram, 1987; Saunders, 1990) and the species

Fig. 1. Distribution of Carnaby’s Cockatoo in southwestern Australia, location of study areas and localities mentioned in text. Solid line depicts eastern limit of the species’ distribution and the dashed line describes the 300 mm annual rainfall isohyet.

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D.A. Saunders et al. / Biological Conservation 161 (2013) 1–9

was officially recognised by the Australian Government as endangered (Environmental Protection and Biodiversity Conservation Act 1999) and listed as ‘‘likely to become extinct’’ by the Western Australian State Government (Wildlife Conservation Act 1950). Carnaby’s Cockatoo nests in large hollows in eucalypt trees (Saunders, 1979) and lays one to two eggs, with two being the most common (Saunders, 1982). Although two eggs is the most common clutch size, usually only one chick is raised. In the breeding areas it feeds mainly on the seeds of several genera of Proteaceae, including Banksia, Hakea and Grevillea (Saunders, 1980, 1982), several species of Eucalypt and on invertebrates consuming flowers and seeds of the Proteaceae (Scott and Black, 1981). In the non-breeding areas it has a similar diet, but also feeds on seeds of exotic species such as Pinus spp., Erodium sp. and almonds (Saunders, 1974, 1980, unpublished data). Two populations of Carnaby’s Cockatoo have been studied in detail (Fig. 1). One population at Coomallo Creek (30°080 S; 115°300 E) was monitored each year from 1969 to 1976 (Saunders, 1982) with many visits to the area each breeding season checking all known nest hollows each visit and searching for new hollows. From 1977 to 1996 this population was monitored during 13 of those breeding seasons using the survey protocol described by Saunders and Ingram (1998). This involved visiting the area in the second week in September and the second week in November, checking all known nest hollows in the area and searching for new nest hollows. From 2009 to 2011 the Coomallo Creek population was again monitored using the September and November survey protocol. Data for egg-laying of the Coomallo Creek population from the 24 breeding seasons 1969–1978, 1981–1986, 1988– 1990, 1994, 1996 and 2009–2011 were used in our analyses. The second population was at Manmanning (30°510 S; 117°060 E). This population was studied from 1969 to 1976 (Saunders, 1982). Data from 1969 were incomplete, so this year was not used in these analyses. This population disappeared from the area in 1977 (Saunders, 1982, 1986) as a result of detrimental impacts of broad-scale clearing for agriculture. 2.3. Calculation of egg-laying dates At both Coomallo Creek and Manmanning, the length of the folded left wing of each nestling was measured. Each nestling was then aged using a known correlation between age and wing length as described by Saunders (1986). Using the estimated age, the nestling’s laying date was extrapolated based on an incubation period of 28 days (Saunders, 1982). Only the laying dates for the first egg in each clutch were used in our analyses. Laying dates of first eggs in each clutch were grouped into weeks, with week 1 being 1–7 January. Data analysed in relation to rainfall were the weeks the first eggs were laid during each breeding season at Coomallo Creek and Manmanning. 2.4. Rainfall data Rainfall data for each year for which egg-laying dates were available were taken from Bureau of Meteorology data for Badgingarra Research Station (http://www.bom.gov.au, Station Number 009037, accessed 28 June 2011). Badgingarra is on the Swan coastal plain and is within an area where the Carnaby’s Cockatoo Coomallo Creek population spends most of the non-breeding season (Saunders, 1980). The rainfall data from Badgingarra were also used in analyses of the Manmanning egg-laying dates. This was appropriate as the Manmanning population also spent much of its non-breeding season on the Swan coastal plain, to the southwest of Badgingarra. Badgingarra provides rainfall records representative of much of the non-breeding area range of the Manman-

Table 1 Comparison of eight candidate linear and non-linear regression models fitted to the egg-laying and rainfall data from Coomallo Creek and Manmanning sites. Models were evaluated according to Akaike’s Information Criterion (AIC; column 2). The AICbest model (in bold) fits a simple linear relationship between the commencement of egg-laying and the sum of the rainfall in the first half of autumn for Coomallo Creek and autumn rain for Manmanning. First half of autumn includes weeks 9–16, autumn includes weeks 9–22. The deviance reduction (3rd column) of each model represents the amount of variation in the commencement of the egg-laying explained by variation in the independent variable given in the model statement (first column). Deviance reduction is measured relative to the null model that includes only an intercept term. Regression model coefficients for the influence of rainfall in the first half of autumn and all of autumn on commencement of egg-laying were all significantly different to zero (p < 0.001) for both locations. Model equation

AIC

Deviance reduction (%)

Coomallo Creek first egg  a + first.half.autum.rain first egg  a + sqrt(first.half.autum.rain) first.egg  a + autumn.rain first egg  a + log(first.half.autum.rain) first egg  a + log(autumn.rain) first egg  a + second.half.autum.rain first egg  a + log(second.half.autum.rain) first egg  a

86.53 87.23 91.54 92.05 95.41 101.0 102.3 104.3

56 55 46 43 37 20 15 –

Manmanning first.egg  a + autumn.rain first egg  a + log(autumn.rain) first egg  a + first.half.autum.rain first egg  a + sqrt(first.half.autum.rain) first egg  a + log(first.half.autum.rain) first egg  a + second.half.autum.rain first egg  a + log(second.half.autum.rain) first egg  a

23.19 23.56 25.51 25.56 26.13 28.52 29.56 29.39

59 58 57 56 55 32 15 –

ning population. Rainfall records were grouped in weeks, again with week 1 being 1–7 January. 2.5. Statistical methods Generalized linear models (GLMs) with a Gaussian link were used to model the relationship between the timing of first egg-laying in any given year and the amount of rainfall received in various periods during that year (Table 1). Regression models were fitted in the freeware statistical package R (version 12.2; R Development Core Team, 2010). A total of eight candidate models indicating the period of rainfall most influential on the timing of egg-laying, all fitted with three transformations of the independent (rainfall) variables (Table 1) were fitted to the Coomallo Creek and Manmanning data for first eggs laid. The performance of each model was evaluated using Akaike’s information criterion (AIC) (Akaike, 1973) which seeks to optimise the trade-off between the ability of the model to explain the variation in the dependent variable and the complexity of the model, measured by the number of fitted parameters. We recorded the amount of variability explained by each model by looking at the percentage of deviance reduction achieved by each model compared with the null (intercept-only) model.

3. Results 3.1. Commencement of egg-laying and rainfall Over the 43 year period (1969–2011) at Coomallo Creek there was a 7 week difference between the earliest commencement of egg-laying (week 27 in 1974 and 1984) and the latest (week 34 in 1978) (Table 2). In the 7 years 1970–1976 at Manmanning there was a 4 week difference between the earliest and latest commencements (week 31 in 1974 and week 35 in both 1972 and 1973) (Table 2). Egg-laying started later each year at Manmanning

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D.A. Saunders et al. / Biological Conservation 161 (2013) 1–9

Table 2 Number of first eggs laid each week at Coomallo Creek (1969–2011) and Manmanning (1970–1976). The weeks during which the median eggs were laid each year are indicated in bold. The differences between the start of laying at Coomallo Creek and Manmanning each year are also shown (Diff CC&M in weeks). Wk

Dates

Coomallo 27 July 3–9 28 July 10–16 29 July 17–23 30 July 24–30 31 July 31–August 6 32 August 7–13 33 August 14–20 34 August 21–27 35 August 28–September 3 36 September 4–10 37 September 11–17 38 September 18–24 39 September 25–October 1 40 October 2–8 41 October 9–15 42 October 16–22 43 October 23–29 44 October 30–November 5 45 November 6–12 46 November 13–19 47 November 20–26 Total Manmanning 31 July 31–August 6 32 August 7–13 33 August 14–20 34 August 21–27 35 August 28–September 3 36 September 4–10 37 September 11–17 38 September 18–24 39 September 25–October 1 40 October 2–8 41 October 9–15 42 October 16–22 43 October 23–29 Total Diff CC&M

69

70

2 1 1 3 1

1

1 2 4 4 3 2 4 2 1 2 2

71

2 8 4 3 9 3 3 4 6 1 1

1

72

5 14 11 7 5 9 9 1 1 1

73

6 12 12 11 5 8 2 3 4 4 2 2

74 1 1 4 7 5 10 10 6 4 4 4 5 1 2 3 3 2

75

1 7 3 15 5 7 5 8 4 3 3 1 3 3 1

76

77

78

81

82

83

2 2 2 15 5 6 6 4 4 3

1 3 2 4 5 8 1 3

2

1

2 5 3 4 4 3 3 1 1

2 4 9 4 1 1 2 1 1

3 6 2 4 4 2 8

1 1

2 8 11 2 1 1 1 2 1 2

84 1 1 4 2 1 5 6 2 1 1 2 2 4

85

86

88

89

90

1 2 4 5 7 9 3 1 2 1 1 2

3 3 10 5 1 7 2 1 2 2 1

1 1

94

96

9

10

2 1 2 4 10 3 9 6

1 2 3

2 11 7 7 6 2 2 4

2 4 7 2 3 5 4 3 3

1 5 1 5 3 1 1

7 6 4 1 1 1

2 1

2 1 1

1 3

1

3 2 7 3 6 3 3 4

2 4 4 4 3 6 3 4

1 1

2 1

1 1

1

27

2 1 4 3 2

45

1 6 5 1 3 1 1 1

1

13 2

19 4

63

1 2 5 2

71

2 1

1

3 1 2 1

11 3

1 11 4

1 73

69

1 1

1

1 7 1 1

12 4

2

51

28

27

26

31

31

32

40

44

38

37

39

2 4 4 14 7 2

3 1

1

9

11

20

24

35

34

37

1 1

1 1 2

3 1

7 3

6 4

than Coomallo Creek with the difference ranging from 2 to 4 weeks (Table 2). At both Coomallo Creek and Manmanning there was a significant relationship between the commencement of egglaying each season and the sum of the rainfall in the first half of autumn (weeks 9–16) of that year (Fig. 2). The median date of egg-laying each season demonstrated a similar relationship with the sum of rainfall in the first half of autumn of that year. The relationships between the timing of commencement of egglaying and the rainfall in various time periods were examined statistically with a range of competing GLMs. The AIC-best model (Table 1) for both data sets comprised a simple linear model in which the sum of the rainfall in the first half of autumn had a statistically significant (p < 0.0001) negative influence on the commencement of egg-laying, measured as the number of weeks since the start of the year. The effect-size of this relationship was biologically significant in both places. A 100 mm increase in rainfall in the first half of autumn gives rise to a 5 week reduction in the commencement of egg-laying at Coomallo Creek and a 3 week reduction at Manmanning (Fig. 3). While the models based on the sum of rainfall in the first half of autumn were the AIC-best models, there was some uncertainty about whether or not the simple linear model was favoured over the model that contained a square root transformation of the rainfall variable. However, the practical difference between the two models, in terms of how differently they predict the commencement of egg-laying in relation to rainfall in the first half of autumn

is minimal. Accordingly, we favour the simple linear model for ease of interpretation. 3.2. Length of the egg-laying period The length of the egg-laying period at Coomallo Creek varied from 10 weeks in 1994 to 21 weeks in 1974 with a median of 12 weeks. The period of egg-laying was shorter at Manmanning and varied from 5 weeks in 1976 to 9 weeks in 1972 with a median of 8 weeks. At Coomallo Creek the egg-laying period was longer in years where egg-laying commenced in the 4 weeks from the earliest recorded laying (weeks 27–30) compared with the latest 4 weeks (weeks 31–34) (Table 2). Egg-laying commenced in weeks 27–30 in 10 years during which the period of egg-laying varied from 11 to 21 weeks with a median of 13 weeks. Egg-laying started in weeks 31–34 in 13 years with a range of 10–15 weeks and a median of 11 weeks (Table 2). There was no trend at Manmanning in length of egg-laying period and commencement of egg-laying. 3.3. Commencement of egg-laying by individual females Data on egg-laying over successive seasons are available from 95 individually marked females from Coomallo Creek and 15 from Manmanning. Data from Coomallo Creek included 55 sets with two successive breeding seasons, 34 with three, 10 with four, four with five and one with eight. As the population at Coomallo Creek was not surveyed every year, several females provided data for succes-

5

34

'78

'72 '94

'96

'70

'77 '81

'83 '82 '85

'73

2009

30

31

32

33

2011

'76

'69

29

'89

'88

2010 '90 '71

28

(a)

'86

'75

27

(a)

commencement of egg laying (week no.)

D.A. Saunders et al. / Biological Conservation 161 (2013) 1–9

'84

0

20

40

60

'74

80

100

120

1970

1971

1972

1973

1974

1975

1976

year Fig. 2. Relationship between commencement of egg-laying (solid lines) and the first half of autumn rainfall (broken lines) for (a) Coomallo Creek (1969–2011) and (b) Manmanning (1970–1976). To aid visual interpretation, the timing of egg-laying (y-axis) is represented as the number of weeks before the end of the year (i.e. 52 – the week of egg-laying). The dashed portion of the egg-laying curve indicates an 8 year gap in nest surveys.

sive seasons, then after years not surveyed, further data from successive seasons. For example, one female (identified by patagial tags with letters UC) provided data for 4 years 1974–1977 and again from 1981–1984; that is two sets of four successive seasons. Data from Manmanning included seven females with two successive breeding seasons, three with three, three with four and two with five. At Coomallo Creek, in relation to the commencement of egg-laying each season, females laid their first egg from 11 weeks before they did the previous year to 11 weeks after. At Manmanning this range was 6 weeks before until 6 weeks after (Fig. 4). At Coomallo Creek, in relation to the start of the egg-laying period for the population, 47% of females laid their first egg in the range of 1 week before until 1 week after they did the previous year. Sixty-two percent laid their first egg in the range of 2 weeks before and 2 weeks after. At Manmanning, 50% of females laid within the range of 1 week before and 1 week after and 75% in the range 2 weeks before to 2 weeks after (Fig. 4). Data on commencement of egg-laying are available for 22 individually marked females from Coomallo Creek and five from Manmanning with more than three breeding seasons (Table 3). These data show that

35

'73

'70

'76

32

33

34

'72

'71

'75

31

200 100 0

10

50

150

20 15

250

25

300

(b)

first half autumn rainfall (mm)

week of commencement of egg-laying

(b)

commencement of egg laying (week no.)

rainfall in the first half of autumn (mm)

'74

100

150

200

rainfall in autumn (mm) Fig. 3. Predicted versus observed timing of commencement of egg-laying for (a) Coomallo Creek (1969–2011) and (b) Manmanning (1970–1976). Predictions for commencement of egg-laying (solid line) are obtained from the AIC-best model that quantifies the relationship between commencement of egg-laying and rainfall in the first half of autumn for Coomallo, and the whole of autumn for Manmanning. Observations of commencement of egg-laying each year plotted against the rainfall in the relevant period of that year are given as open circles. The year of each observation is indicated.

there is no tendency for the older, and therefore the more experienced, females to breed earlier in the season than younger females. Carnaby’s Cockatoo begins breeding at 4 years of age (Saunders, 1982; Saunders and Ingram, 1998). Data on commencement of egg-laying are available for four known aged females at Coomallo Creek the first year they bred. All were banded as nestlings at Coomallo Creek. One laid 2 weeks after the start of the breeding season, one in the fourth week and two in the eighth week. Data are available from 12 individually marked females who made two breeding attempts in one season. All moved to new nest hollows after failing in the first attempt. One laid 1 week after failing, one 3 weeks later, three 6 weeks later, one 7 weeks later, four 8 weeks later, one 9 weeks later and one 11 weeks later. The average was between 6 and 7 weeks after the failed clutch was laid. 3.4. Commencement of egg-laying in offspring compared with their female parent Data on several laying dates are available for only two females of known age and for their female parent. 01694 (band/ring num-

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D.A. Saunders et al. / Biological Conservation 161 (2013) 1–9

Fig. 4. Number of weeks individual females laid their first egg for the season in relation to their first egg the previous season for 95 individually marked females from Coomallo Creek (black: ranging from two to eight successive years) and 15 from Manmanning (grey: two to five successive years).

Table 3 Data on the commencement of egg-laying of 22 individually marked females from Coomallo Creek and five from Manmanning for which there are records for at least three breeding seasons. Data are the number of weeks after the commencement of egg-laying for that season the bird laid her first egg. 0 is the first week of egg-laying in the season. Letters indicate females marked with patagial tags and numbers indicate those with leg bands only. The year in brackets indicate the year the bird was individually marked and 4+ indicates that it was an adult when marked. 4 and 19 indicates the birds were banded as nestlings and were therefore known aged individuals. In some cases the birds had two breeding attempts in a season and these are indicated. 69 Coomallo Creek AN (4+ 1970) EF (4+ 1972) SN (4+ 1972)

70

71

72

73

74

75

76

77

6

3

3 2 4

3 6

4

3 6 5

7 5 4

3 4 5

5 5

4 5

4 7

3 4 7 1st 3 2nd 14 7 1 1st 2 2nd 8 3

8 7

7 5

7

2

1st 5 2nd 14

MI (4+ 1973) MJ (4+ 1973)

2 3

MH (4+ 1973) MP (4+ 1973) MX (4+ 1973) MW (4+ 1973)

3 4 4 5

MY (4+ 1973) UE (4+ 1974) UC (4+ 1974)

5

UF (4+ 1974) US (4+ 1974)

1st 5 2nd 11 7 3 6 5 6 1 2 3 5

4 0 4 4 1st 4 2nd 12

03143 (4+ 1985) 03010 (4+ 1985) 03011 (4+ 1985) 01596 (4 1986) 01876 (4+ 1988) 1652 (4+ 1989) 03089 (4+ 1994) 01694 (19 2009) Manmanning BP (4+ 1969) BT (4+ 1969) BL (4+ 1970) BC (4+ 1971) OF (4+ 1973)

78

81

82

83

84

2

3

2

5

2

1

0

6

2 2

7 6

85

86

88

89

7

9

4

2

90

94

2 4 4

3 1 1

5 3 2

5

8

7

4

8

9

8

8

8

3

4

4

5

2

1

5

4

5

9

4 10

4

2

2

8 9

4 2

11

4

2

2 4 4 0

10

2

4

4 7

9

6

8

5 5

96

4 5 3 1

3

5

4 1

5 3

1

ber) was 19 years old in 2009 when she laid in the fourth week after the first egg laid for the season. In 2010 and 2011 she laid

in the second week. In 1986 her female parent 01596 laid in the eighth week, in 1988 the fourth week, 1989 the third week and

D.A. Saunders et al. / Biological Conservation 161 (2013) 1–9

1990 the fourth week. 03114 was five in 1989 when she laid in the fifth week. In 1990 she laid in the ninth week. Her female parent 01463 laid in the 11th week in 1984, and the fifth week in 1985 and 1988.

4. Discussion 4.1. Commencement of egg-laying and autumn rainfall It is clear from this study that commencement of egg-laying in Carnaby’s Cockatoo is strongly influenced by autumn rainfall, with later commencement of egg-laying in years which have less rainfall in the first half of autumn. In addition, the later the commencement of egg-laying, the shorter the period over which eggs are laid (Table 2). Autumn rainfall provides a cue to fine-tune their breeding. This makes strong biological sense as autumn rainfall mediates flower and seed set in the Proteaceae that make up the primary nutritional source for breeding birds, allowing them the opportunity to raise their young when most food should be available. However, given that the species of Banksia that form a significant part of their diet during the breeding and non-breeding season take 2.5– 7 months to develop flower buds (usually in winter-early spring), flower for 4–7 months depending on species, and then the seed follicles take a further 1–2 years to develop (George, 1987; Taylor and Hopper, 1988) the influence of rainfall on food plants is not in synchrony with the response of the cockatoos to autumn rainfall. Carnaby’s Cockatoo lives in a region with hot-dry summers and cool-wet winters. Although rain falls mainly in the cooler period of the year, there is considerable annual variability. For example, during 1994, the driest year of the study, rainfall at Badgingarra was 65% of the long-term mean rainfall and during 1974, the wettest year, was 126%. Our results indicate that at Coomallo Creek, over the period 1969–2011, there was no trend in commencement of egg-laying that would indicate that the breeding season is starting later or earlier this century, than it did in the 1970s and 1980s (Fig. 2). While rainfall in the first half of autumn may be the cue for Carnaby’s Cockatoo to time its breeding, this cue must set in train physiological and behavioural changes in individuals. Physiologically the birds must prepare themselves for producing eggs and sperm. Behaviourally, they must reinforce their pair bonds, return to their breeding areas, select and prepare a suitable nest hollow and lay their first egg. Obviously, all birds are not programmed to respond to the rainfall cue within the same time frame. The timing of egg-laying in individual birds may also be influenced by the amount and quality of food available to them during the nonbreeding season. One piece of evidence of individual variation in responses is that all pairs do not return to their breeding areas at the same time. Saunders (1980) described how some individuals from the Manmanning breeding population were still in the nonbreeding area in late August, while others from that population were commencing to breed. This was also true of individuals from the Coomallo Creek population (Saunders, unpubl. data). The period over which eggs are laid is also evidence of the range of the responses of individuals to the cue. For example, at Coomallo Creek in 1974 the first eggs of the breeding season were laid in week 27 and the last in week 47, a period of 5 months (Table 2). Interestingly, in that season, one nest hollow was used by two separate pairs and each successfully fledged a nestling. The first pair laid their first egg on 17 July (week 28) and the nestling fledged by 5 November (week 44). The second pair laid their first egg on 21 November (week 47) and the nestling had successfully fledged by early March; almost continuous occupancy of the nest hollow for eight and a half months.

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4.2. Egg-laying by individuals in relation to the commencement of egglaying each season The difference between individual females in how they respond to cues to time their breeding was shown by the times they laid in relation to the commencement of egg-laying by the population in each study area. At Coomallo Creek, 62% of egg-laying by individuals was within the range of 2 weeks before or 2 weeks after the previous year’s egg-laying date and at Manmanning the figure was 75%. This indicates that individuals were relatively consistent over time in laying their first egg at the same time in relation to the commencement of each season’s egg-laying by the population (Fig. 4 and Table 3). The timing of egg-laying was apparently not a function of age. Intuitively, it seems logical that the older, more experienced females would be expected to lay their egg earlier than younger females in order to maximise their choice of nest hollows and food. This did not appear to be the case, as females breeding for the first time laid their first egg from 2 to 8 weeks after the commencement of the laying season, some older birds laid early and others later. For example, at Coomallo Creek, one marked female (UF) who was banded as an adult (and therefore was at least 4 years old) laid her first egg for the season in the first half of the season from 1974 to 1983, but laid in the second half of the season from 1984 to 1989, by which time she was at least 16 years old. In contrast, another female (UC) which was banded as an adult in 1974 laid her first egg in the first half of the season for the eight seasons she was recorded breeding, by which time she was at least 12 years old (Table 3). Five percent of egg-laying by individuals was within the range of 6–11 weeks before or 6–11 weeks after they commenced the previous season. These large differences were most likely to have been the result of a second attempt after their first attempt had failed. For example, a female commencing to lay in one season 11 weeks before she had the previous season, may have failed in her first attempt the previous season and the comparison was with her second attempt the previous season with her first attempt the following season. Our survey protocol involved only checking nest hollows twice a breeding season and may not register every breeding attempt by individuals. 4.3. Is timing of egg-laying in offspring similar to their female parent? With only two females of known age whose female parent’s breeding history is partly known, there are few data to examine this question. While the data are limited, they suggest that offspring tend to commence egg-laying each season at a similar time as their female parent. 4.4. Differences in commencement and length of egg-laying between study areas The areas the Coomallo Creek population spend their nonbreeding season were within 30 km of their breeding area and many of them less than 20 km away (Saunders, 1980). This is a distance that birds which still have nestlings will commute to feed with the rest of the flock that have finished breeding and moved to their non-breeding foraging areas (Saunders, unpubl. data). The population breeding at Manmanning spent the non-breeding season in areas over 100 km from their breeding sites. Saunders (1980) noted that the shortest time recorded for an individual from Manmanning leaving Yanchep (one of its non-breeding foraging areas) and appearing at Manmanning at the start of the breeding season was 13 days. With the birds of the two populations responding to the similar rainfall cues, it is possible that the later commencement of egg-laying at Manmanning compared with Coo-

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mallo Creek was a function of the difference in distance between the non-breeding foraging areas and the breeding areas of the two populations. The difference in the length of the egg-laying period between the two populations may have been a function of population size; the larger the population, the longer the egg-laying period. The Manmanning population in 1971 had 19 breeding attempts. The study area had been thoroughly searched for tree hollows by 1971 and most breeding attempts would have been recorded. On the other hand, the Coomallo Creek study area was still being expanded and new hollows added by 1973. So the 70+ breeding attempts in the mid-1970s represent a reasonable indicator of population size; nearly three and a half times the size of the population at Manmanning.

4.5. Conservation implications under a predicted changing climate Predictions of climate change for southwestern Australia are that the region is likely to be hotter and drier. CSIRO (2007) reported that ‘‘droughts are likely to become more frequent particularly in the southwest.’’ Hennessy et al. (2008, page 28) reported that ‘‘in southwest WA (SW WA), the frequency and areal extent of exceptionally hot years and exceptionally dry years are likely to increase in the future. . .. . .The mean projections indicate that: by 2010–2040, exceptionally hot years are likely to affect about 80% of the region, and occur every 1.2 years on average; by 2010–2040, exceptionally low rainfall years are likely to affect about 18% of the region about every seven years on average’’. What are the implications of these changes on the breeding of Carnaby’s Cockatoo? It is known that Carnaby’s Cockatoo is susceptible to heat stress. Saunders (1982) reported that during very hot weather (>35 °C) the species could not forage and sat in the foliage of trees out of the sun during the heat of the day. Very hot weather reduces the time available for foraging and drinking and can exacerbate the impacts of any food shortages. Saunders et al. (2011) reported on the impacts of one very hot day on the south coast of Western Australia in January 2010 during which 208 Carnaby’s Cockatoo were killed by heat stress in two locations when the maximum temperature was 48 °C. More extreme hot weather will expose the birds to more such events. Carnaby’s Cockatoo uses rainfall in the first half of autumn as a cue to prepare for egg-laying in winter and spring. The heavier the rainfall, the earlier egg-laying commences. If predictions of southwestern Australia being drier in future mean a decrease in autumn rainfall, this may mean that egg-laying will commence later in the year and, as shown by the population at Coomallo Creek, breeding seasons may be shorter under drier and hotter conditions. The incubation period of Carnaby’s Cockatoo is 4 weeks and the nestling period 10–11 weeks (Saunders, 1982). Each pair needs 14– 15 weeks from the time the first egg is laid until the resulting nestling leaves the nest hollow and they can move to the non-breeding foraging areas. Incubation and nestling periods are unlikely to change as a result of any change in climate. If predictions of more hot weather are correct, this may mean that birds laying eggs later in the breeding season (from September on) will be trying to raise their nestlings in hotter weather than at present. This may mean that when its energetic demands are highest, there is less time to forage. In addition, they are foraging further from their nest sites because food closer to the nest sites may have already been depleted. The result may be that birds laying their eggs later in the season will not be successful because of the combination of diminution of foraging time and the impact of hot weather on adults and nestlings. At Manmanning in the final years before the population disappeared from the area, the combination of shortages of food and hot weather meant that the successful pairs were only

those that laid their eggs in the first half of the breeding season (Saunders, 1982). A shorter breeding season may also mean that opportunities for relaying after a failed first breeding attempt will be reduced. Individuals at Coomallo Creek have successfully bred after failing in their first breeding attempt. This may not be possible under a hotter and drier climate. It is possible that climate change could provide strong selection pressure that acts on individuals and the timing of egg-laying. The individual variability may provide the species with adaptive capacity such that early egg-laying is favoured and the population responds accordingly. Saunders et al. (2011) pointed out that under predictions of climate change in southwestern Australia, the range of Carnaby’s Cockatoo will contract as the arid zone moves much closer to the coast. Any contraction of a range, which has already decreased by over 30% over the past 40 years as a result of broad-scale clearing of native vegetation, combined with any contraction of the period each year available for successful breeding, may push this already endangered species closer to extinction.

Acknowledgements We would like to thank John Ingram, formerly of CSIRO Wildlife Research, for technical support during the research at Coomallo Creek (until 1996) and Manmanning. All field work until the end of 1996 was conducted under appropriate ethics and banding permits held by Denis Saunders and from 2003 under appropriate ethics and banding permits held by Peter Mawson. Fig. 1 was prepared by Abby Thomas. We are grateful to Lynda Chambers, Stephen Garnett, Lesley Hughes, Harry Recher, an anonymous reviewer and Tracey Regan (the journal handling editor) for constructive criticism of earlier drafts of this paper. Brendan Wintle was supported by an ARC Future Fellowship.

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