Climate and Vegetation Changes at Coringa-Herald National Nature Reserve, Sea Islands, Australia1

George N. Batianoff,2 Gillian C. Naylor,2 John A. Olds,3 Nigel A. Fechner,2 and V. John Neldner2,4

Abstract: Climatic changes at Coringa-Herald National Nature Reserve (CHNNR) in the last 82 yr include a 0.7C rise in mean minimum winter tem- peratures and increases in drought duration and frequency. Between 1991 and 2002, a plague of the scale Pulvinaria urbicola (Cockerell), together with attendant ants destroyed grandis R.Br. rain forest at South-West Coringa Islet. Scale damage of P. grandis has also been recorded at North-East Herald . This study explored the reasons for vegetation dieback during cur- rent climate. Woody species such as Argusia argentea (L.) Heine, Cordia subcor- data Lam., and the grasses Lepturus repens (G. Forst.) R.Br. and Stenotaphrum micranthum (Desv.) C. E. Hubb. have also declined at CHNNR. Ximenia amer- icana L. and Digitaria ctenantha (F. Muell.) Hughes were found to be locally ex- tinct. Dieback of forests results in reduction of canopy-breeding seabirds and burrowing shearwaters (Puffinus pacificus [Gmelin)]. Dieback species were re- placed by the shrub Abutilon albescens Miq. and/or fleshy herbaceous such as Achyranthes aspera L., albiflora Fosberg, micrantha Roem. & Schult, Portulaca oleracea L., and Tribulus cistoides L. Increasing duration of droughts and increased temperatures, together with damage caused by exotic in- sect pests, appear to be the key drivers of the current vegetation changes.

Coringa-Herald National Nature Reserve 125 ha (Batianoff et al. 2009). The remote- (CHNNR), located about 400 km east of ness of CHNNR has safeguarded this area , forms part of the northern Australian from high levels of human disturbance. It Islands Territory. It includes three was declared a National Nature Reserve in groups of cays and islets: the Her- 1982 because it provides critical breeding ald Cays, the Coringa Islets, and the Magde- habitat for colonies of large numbers of nest- laine Cays. The total vegetated area is around ing seabirds and turtles (Environment Austra- lia 2001). According to Batianoff et al. (2009) these northern provide im- portant wildlife linkages between the Great 1 The Commonwealth Department of the Environ- Barrier and the Melanesian islands by ment, Water, Heritage, and the Arts provided financial the influence of the prevailing currents and support and permission to publish results of our studies. Manuscript accepted 19 February 2009. winds (Figure 1). 2 Herbarium, Department of Environ- CHNNR terrestrial ecosystems have been ment and Resource Management, Mt. Coot-tha Road, studied by various biologists including Heat- Toowong, Queensland 4066, . wole (1979), Hicks and Hinchey (1984), 3 Queensland Parks and Wildlife, Department of En- Hicks (1985), Hinchey and Stokes (1987), vironment and Resource Management, P.O. Box 3130, Red Hill, Rockhampton, Queensland 4701, Australia. Donaldson (1994), the Royal Geographical 4 Corresponding author (e-mail: John.Neldner@derm Society of Queensland (2001), Batianoff .qld.gov.au). (2001a,b; unpubl. data), Smith and Papacek (2001a,b,c), Smith et al. (2004), Freebairn (2006a,c,d, 2007), Batianoff and Naylor Pacific Science (2010), vol. 64, no. 1:73–92 doi: 10.2984/64.1.073 (2007), Greenslade and Farrow (2007), Ba- : 2010 by University of Hawai‘i Press tianoff et al. (2009), Greenslade (2008); J. All rights reserved Hicks, unpubl. data; and P. O’Neill, J.A.O.,

73 74 PACIFIC SCIENCE . January 2010

Figure 1. Location of Coringa-Herald National Nature Reserve and within the Coral Sea Islands Ter- ritory showing major currents (arrows) operating within the region (derived from Smith [1994]). and R. Elder, unpubl. data. These surveys re- Severe defoliation of P. grandis from the vealed that dieback of forests dominated by larvae of the Australian native hawkmoth, , Argusia argentea, and Cordia velox, has also been reported at subcordata has occurred over the last few de- CHNNR (Donaldson 1994, Freebairn cades along with several other environmental 2006a,c,d, 2007). The dieback of A. argentea changes. The dieback of P. grandis due to the and C. subcordata is more localized to the effects of plague Pulvinaria urbicola scale in- CHNNR. festations during the last two decades has At CHNNR, insect damage to P. grandis been widely reported at CHNNR (Smith and to a lesser extent to C. subcordata is well and Papacek 2001a,b,c, 2004, Smith et al. documented (Smith and Papacek 2001a, 2004, Batianoff and Naylor 2007, Greenslade Smith et al. 2004, Freebairn 2006a,c,d, 2007). 2008; P. O’Neill, J.A.O., and R. Elder, un- The use of the Australian native Cryptolaemus publ. data) and elsewhere across the Pacific montrouzieri (Molsant) as a biological control and Indian oceans (Handler et al. 2007; A. agent to control the population of plague P. Kay, J.A.O., R. Elder, and K. Bell, unpubl. urbicola scale infestations at North-East Her- data; J.A.O., K. L. Bell, and R. J. Elder, un- ald Cay was outlined by Smith and Papacek publ. data; J.A.O., R. J. Elder, R. M. Charles, (2001a,b,c) and Freebairn (2006a,c,d, 2007). J. R. Platten, and K. L. Bell, unpubl. data). Freebairn (2006a,c,d, 2007) also discussed the Climate and Vegetation Changes at Coringa-Herald . Batianoff et al. 75 use of two species of egg parasitoid (Tricho- tion no. 200283 located at Willis Island (16 gramma pretiosum and Trichogramma carverae) 29 0 S, 149 070 E) (Batianoff and Naylor to control H. velox outbreaks. Continuous 2007, Batianoff et al. 2009, Bureau of Meteo- drought conditions have been shown to in- rology 2008a). Rainfall trends were deter- duce the dieback of in northern Aus- mined by comparing annual rainfall with the tralian savannas (Fensham et al. 2009). long-term mean. ‘‘Dry’’ years were those Droughts have also been linked to explosions when rainfall was below the long-term mean, in pest insect plagues and dieback by as well as those within 50 mm above the mean White (1969). Greenslade (2008) suggested (Batianoff and Naylor 2007). The duration that Pisonia dieback at CHNNR may have of droughts was extrapolated by the number been exacerbated by drought stress and nutri- of consecutive ‘‘dry’’ years (Batianoff et al. ent stress due to reduced populations of nest- 2009). However, Willis Island rainfall data ing seabirds. Both of these stressors may be from September 2004 to October 2006 are indirectly caused by climatic trends. The aim not available due to the upgrading of moni- of this study is to examine the role of climatic toring equipment (Bureau of Meteorology trends over the last two decades in relation to 2008a). We were not able to fill this gap vegetation changes and with reference to de- from other sources because there is no off- pendent wildlife at CHNNR in accordance shore rainfall data available for nearby areas. with international climate knowledge (Inter- As a result, some of the interpretation of governmental Panel on Climate Change droughts during that period is based on ob- 2007). servations of vegetation condition (Batianoff On coral cays, vegetation structure and et al. 2009). individual plants are important in provid- A drought index (Dm; y) was calculated for ing ‘‘functional’’ diversity (Walker and Salt each month m of each year y based on the 2006). Some of these functions include actual annual rainfall for 3 yr before every landform development, habitat diversity for month less the expected (long-term average) wildlife (including invertebrates [Greenslade rainfall for that period, divided by the mean and Farrow 2007, Greenslade 2008]), and annual rainfall: nesting/roosting and/or shelter for a large number of seabirds (Batianoff 2001a,b, Ba- Xy am; y A tianoff and Cornelius 2005). In particular, A. D ; ¼ ; m y A argentea and P. grandis communities at i¼yxþ1 CHNNR form critical nesting habitat for the arboreal and ground-nesting seabirds. where am; y is the summed monthly rainfall More than half of the breeding seabirds at over the previous 12 months of year y (that CHNNR utilize these woody species. For ex- is, from month m to m-11), and A is the ample, the Lesser and Great Frigatebirds long-term annual average rainfall (for Willis (Fregata ariel, F. minor), the Common Noddy Island it was averaged over 82 yr). Three (Anous stolidus), the (Anous min- years was chosen as deficit period, x. The Fo- utus), the Red-footed Booby (Sula sula), as ley Index of drought (Foley 1957) was chosen well as the burrowing Wedge-tailed Shear- over other drought indices for reasons out- water (Puffinus pacificus) are the most com- lined in Fensham et al. (2009). That is, it can mon breeding seabirds utilizing Pisonia and be calculated for any period and only requires Argusia stands (Batianoff 2001a). rainfall data. Trends in ambient temperatures were de- termined by comparing the mean maximum materials and methods and minimum temperatures for summer and winter months for each decade since 1925– Climate Trends 1934 (Batianoff et al. 2009). Unless otherwise Climate data for the region were extrapolated stated, all references to seasons are to the and are presented in this paper from 82 yr of standard Australian allocation of months records from the Bureau of Meteorology sta- (i.e., summer is from December to February, 76 PACIFIC SCIENCE . January 2010

Figure 2. Mean monthly rainfall anomalies from the long-term monthly mean of 93 mm at Willis Island, 1922–2007 (Batianoff and Naylor 2007, Bureau of Meteorology 2008a). autumn from March to May, winter from results and discussion June to August, and spring from September to November. Data were accurate up to 31 Current Climatic Trends July 2008. The northern Coral Sea Islands Territory study area experiences a dry, tropical mari- time climate. According to Mueller-Dombois Vegetation Changes and Fosberg (1998), Willis Island, with a mean annual rainfall of 1,115 mm is a ‘‘dry is- The effects of climate on vegetation and as- land.’’ According to Batianoff and Naylor sociated wildlife at CHNNR are based on (2007) the current climate patterns include three terrestrial surveys from 1997 (Batianoff 3–4 months of ‘‘wet’’ and 8–9 months of 2001b) and 2006–2007 (Batianoff and Naylor ‘‘dry’’ seasons as well as longer-term patterns 2007, Batianoff et al. 2009). Dieback and of ‘‘dry’’ and ‘‘wet’’ years (Figures 2 and 3). other species turnover were identified using During the summer period, tropical depres- all available data including unpublished re- sions in the zone of convergence between ports ( J. Hicks; P. O’Neill, J.A.O., and R. ‘‘monsoon’’ and ‘‘trade’’ winds bring storms Elder) and personal communications with and cyclonic weather to tropical areas (Far- CHNNR monitoring team leader, M. Hal- row 1984, Myers and Kent 2005). Stoddart lam (1997, 2006, and 2007). These additional and Walsh (1992) reported that the variability data include the extensive reporting on the in rainfall at Willis Island has longer cycles of scale insect infestations of Pisonia grandis by 12–30 yr between wet and dry ‘‘epochs.’’ It is Smith and Papacek and Smith et al. (2001– generally assumed that these fluctuations cor- 2004), Freebairn (2006–2007), and Green- respond with the El Nin˜ o–Southern Oscilla- slade (2008). Other predicted climate change tion (ENSO) and the Inter-decadal Pacific impacts are based on an extensive literature Oscillation (Myers and Kent 2005). Pro- review of tropical regions. The localized ef- longed drought stress in the northern Coral fects of climate change to seabirds on coral Sea region occurs as part of the ENSO phe- cays follow data presented by Batianoff and nomenon. The ENSO phenomenon brings Cornelius (2005), Turner and Batianoff periods of higher rainfall to Australia during (2007), and Baker et al. (2006, 2008). the ‘‘La Nin˜ a’’ phase and drier conditions Climate and Vegetation Changes at Coringa-Herald . Batianoff et al. 77

Figure 3. Annual rainfall at Willis Island, 1922–2007 expressed as deviation from the long-term mean of 1,115 mm (Batianoff and Naylor 2007, Bureau of Meteorology 2008a). due to lower rainfall during the ‘‘El Nin˜ o’’ evaporation. Evaporation data are not avail- phase (Suppiah et al. 2001, Cai et al. 2003). able for Willis Island; however, Farrow Summaries of global current climate (1984) reported that January and April were trends (Intergovernmental Panel on Climate the only months at Willis Island where rain- Change 2007) and regional trends (Suppiah fall exceeded evaporation. Relative humidity et al. 2001, Cai et al. 2003, Hughes 2003, at Willis Island is between 68% and 81% Johnson and Marshall 2007) provide general- (Table 1). ized overviews of climate trends based on the According to Batianoff et al. (2009), be- modeling of large climate data sets from tween 1925–1934 and 1995–2004 the mean many locations. In this study, climate trends minimum temperature at Willis Island has in- are discussed at a local level using one set of creased þ0.7C, though the mean maximum climate data depicting a relatively small tropi- temperature has remained relatively un- cal offshore region (Batianoff and Naylor changed (Table 2). Temperature increase 2007). These data are used to provide proba- has been most pronounced for the mean min- ble explanation for some of the current Piso- imum winter temperature (þ0.7C), with the nia grandis forest and other vascular plants summer minimum temperature increasing dieback at CHNNR (Batianoff et al. 2009). þ0.6C. The mean winter maximum and summer maximum temperatures have re- mained relatively unchanged (Table 2). The Ambient Temperatures and Humidity temperature rises recorded in the study area Ambient temperatures at Willis Island show are lower than for the Australian mainland. little variability throughout the year (Table According to Suppiah et al. (2001), the mean 1). Temperatures are between 25.7C and minimum temperature increase on the main- 30.7C during the warmest month of January, land has been þ0.96C and maximum tem- with the highest temperature recorded at perature þ0.56C in a similar period. 35.2C. The temperature for the coolest month of July ranges between 21.9C and Rainfall 26.0C, with the lowest temperature recorded at 18.9C. The stable and relatively high an- According to Batianoff and Naylor (2007) nual temperatures above 20C result in high most of the annual rainfall at Willis Island 78 PACIFIC SCIENCE . January 2010

TABLE 1 Willis Island Monthly Temperature, Rainfall, Humidity, and Cyclone Data: 1921–2007 (Bureau of Meteorology 2008a,b)

Min. Mean Mean Min. Mean Max. Terrestrial Monthly %of Relative %of Temp. Temp. Temp. Rainfall Total Rain Total Humidity Cyclones Month (C) (C) (C) (mm) Days Rain Days (%) per Month

Jan. 25.7 30.7 24.3 193 10 13 74–78 26 Feb. 25.6 30.4 24.3 226 12 15 78–81 30 Mar. 25.4 29.8 24.1 198 12 15 77–79 19 Apr. 24.7 28.8 23.4 129 9 12 75–77 11 May 23.8 27.7 22.4 76 7 9 74–75 1 June 22.6 26.5 21.1 58 6 8 72–73 0 July 21.9 26.0 20.4 38 5 6 69–71 0 Aug. 21.9 26.3 20.2 24 3 4 68–71 0 Sep. 22.5 27.3 20.9 17 2 3 68–70 0 Oct. 23.6 28.7 22.1 19 2 3 69–71 1 Nov. 24.7 29.9 23.2 36 3 4 69–72 0 Dec. 25.4 30.6 23.9 99 6 8 71–74 12 Average 24.0 28.6 22.5 93 7 — 72–74 —

TABLE 2 Ambient Temperature Increases for Willis Island: 1921–2007 (Bureau of Meteorology 2008a)

Annual Summer Winter

Mean Mean Mean Mean Mean Mean Maximum Minimum Maximum Minimum Maximum Minimum Period Temp. (C) Temp. (C) Temp. (C) Temp. (C) Temp. (C) Temp. (C)

1925–1934 28.4 23.7 30.2 25.4 26.1 21.8 1935–1944 28.7 23.8 30.8 25.6 26.3 21.8 1945–1954 28.6 24.0 30.5 25.5 26.5 22.1 1955–1964 28.8 23.9 30.7 25.4 26.6 22.1 1965–1974 28.6 23.9 30.6 25.4 26.3 22.2 1975–1984 28.6 24.0 30.7 25.6 26.1 22.1 1985–1994 28.4 24.2 30.5 25.8 26.1 22.4 1995–2004 28.7 24.4 30.8 26.0 26.2 22.5 Trend No trend þ0.7C No trend þ0.6C No trend þ0.7C Strong Moderate Strong trend trend trend

occurs during the ‘‘wet’’ summer/autumn mm in 1966 (22% of the mean) to 2,482 mm months of January–April (Figure 2). The in 1997 (223%) (Bureau of Meteorology corresponding ‘‘dry’’ winter/spring months 2008a). Extreme high and low rainfall fluctu- are from May to November, with December ations are generally assumed to correspond recording close to the mean monthly rainfall. with ENSO and/or the Inter-decadal Pacific The rainfall pattern at Willis Island over the Oscillation (Cai et al. 2003, Lough 2007). past 87 yr indicates fluctuating ‘‘wet’’ and However, lower (negative) Southern Oscilla- ‘‘dry’’ periods that may last for 1–7 yr (Figure tion Index values (El Nin˜ o) do not always re- 3). The annual rainfall has varied from 241 late to lower rainfall events in tropical areas. Climate and Vegetation Changes at Coringa-Herald . Batianoff et al. 79

Figure 4. Drought index for Willis Island, 1922–2004. Pest insect population outbreaks at South-West Coringa Islet in 1991 and North-East Herald Cay in 2001. Note that data after 2004 are not available from Willis Island (Bureau of Meteorology 2008a, Foley 1957).

The strong El Nin˜ o event of 1997 was also fall deficits (Figure 3) correspond with yearly the year that Willis Island recorded its high- rainfall deficits (Figure 4) because they high- est rainfall (Bureau of Meteorology 2008a) light the same periods of droughts and in- due to the influence of Jus- tense rainfall. The Drought Index (Foley tin (Bureau of Meteorology 2008b). 1957) of monthly rainfall shows that the According to Batianoff et al. (2009) there most severe drought on record occurred is no discernible long-term trend of changing around 1994, followed by the second most in- rainfall amounts; nevertheless, it is noted that tense rainfall period from 1997 to 2001 (Fig- since 1990, 8 yr have recorded rainfall > 100 ure 4). The worst period of rainfall deficit on mm below the long-term mean (Figure 3). record occurred after 2001. Five years have recorded above-average (me- A moderate trend toward an increase in dian) amounts, and 1 yr has been neutral. drought frequency and duration is apparent Rainfall amounts during the 2004–2006 pe- at Willis Island (Figure 5). The duration of riod were not available for this analysis. How- droughts at CHNNR in the last 43 yr has in- ever, regular visits by field personnel and creased from a mean of 2.3 yr (1922–1964) to examination of oblique air-monitoring pho- 3.3 yr (1965–2007) (Batianoff et al. 2009). tographs indicated continuing ‘‘dry’’ condi- Myers and Kent (2005) predicted drier condi- tions during those periods (Batianoff et al. tions for northern tropical Australia due to 2009). Therefore, we suggest that a continu- projected climate change. However, rainfall ous rainfall deficit occurred from 2001 to projections for the northeastern Queensland 2006. In the 18 yr since 1990, 11 (61%) have region are uncertain due to the limited ability been ‘‘dry,’’ 8 (33%) have been ‘‘wet,’’ and 1 to model the Australian summer monsoon yr (6%) has been ‘‘neutral.’’ (Lough 2007). However, longer durations of The conditions of variable patterns of drought conditions are expected due to the rainfall at CHNNR are illustrated in Figures higher temperatures increasing evaporative 3 and 4. These data show that monthly rain- losses (Lough 2007). 80 PACIFIC SCIENCE . January 2010

Figure 5. Duration of contiguous ‘‘drought’’ years at Willis Island, 1922–2007 (Bureau of Meteorology 2008a). Note that drought years are considered as those years where rainfall is below 1,165 mm (i.e., long-term mean þ50 mm). Data from Willis Island for 2004–2006 are not available; however visiting personnel and oblique aerial photographs taken during that period indicate continued drought conditions (Batianoff et al. 2009).

Wind and Cyclones gion but a slight increase in the intensity of cyclones. Under these conditions, a greater At CHNNR, windy conditions occur 95% of frequency of high winds and storm surges the year (Bureau of Meteorology 2008a). (Hughes 2003) will have direct and indirect The southeasterly ‘‘trade’’ winds make up effects on coral cay ecosystems. 80% and the remaining 20% are known as surges of northerly and northwesterly ‘‘mon- Vegetation Changes soon’’ winds during January to March (Far- row 1984, Bureau of Meteorology 2008a). A During the last two decades, widespread die- total of 184 cyclones has passed within 400 back of trees and annual/short-lived grass km of Willis Island since 1906, with about species across all islands in CHNNR portrays 18 per decade and almost two cyclones per images of environmental stress. As one dom- year (Bureau of Meteorology 2008b). The inant species dies out, the open areas are usual cyclone season at Willis Island is from rapidly colonized by other species, thus main- December to April (Table 2), with February taining vegetation cover and adaptive behav- and January the most cyclonically active ior (Walker and Salt 2006). The replacement months. However, singular cyclone events of Pisonia grandis littoral rain forest with have been recorded within 400 km of Willis herbland/shrubland communities on South- Island in October and May (Bureau of Mete- West Coringa is part of fluctuating seral orology 2008b). stages of coral cay vegetation (Kepler and Long-term cyclone data for Willis Island Kepler 1994, Batianoff 2001b). The replace- indicate a gradual increase in the frequency ment of the rain forest’s structure by low- of cyclones (Batianoff et al. 2009). However, growing vegetation produces a ‘‘normal’’ veg- the number of cyclones recorded at CHNNR etation pattern, be it at a reduced functional for the last decade has been below average diversity. (Bureau of Meteorology 2008b). Hughes This species turnover at CHNNR and/or (2003) reported a slight decline in the num- fluctuating change of dominance between ber of tropical cyclones in the Australian re- different species is an ongoing natural phe- Climate and Vegetation Changes at Coringa-Herald . Batianoff et al. 81 nomenon that provides coral cay resilience to and R. Elder, unpubl. data). During June changing environmental conditions (Heat- 1997, when rainfall was above average (Fig- wole 1979, Kepler and Kepler 1994, Specht ures 3 and 4), G.N.B. recorded healthy and Specht 1999, Batianoff 2001b). However, woody vegetation and a relatively low popula- in the last 20 yr it has been more pronounced. tion of scale insect on Pisonia foliage (Batian- Under current climatic trends, the indigenous off 2001b). The same relatively low levels and exotic insect species (unintentional hu- were also reported in December of the same man introductions) benefit from warmer win- year by P. O’Neill, J.A.O., and R. Elder (un- ters during wet years by the onset of earlier publ. data). However, the scale insect popula- breeding and consequently higher popula- tion at NE Herald had increased by the time tions that damage vegetation (Smith et al. of the 2000–2001 surveys there (Smith and 2004). The increased duration and frequency Papacek 2001a). Between the March and De- of drier seasons favor more drought-tolerant cember 2001 surveys of NE Herald, a 150- and/or disturbance-adapted plant species. fold increase from 1997 values of the scale The increasing plant populations are the population was recorded (Smith and Papacek shrub Abutilon albescens, the perennial grass 2001a,b). The 2001–2002 period also coin- Sporobolus virginicus, and fleshy plants such as cides with a transition from a ‘‘high’’ rainfall Achyranthes aspera, Boerhavia albiflora, Ipomoea phase to a ‘‘drought’’ phase (Figures 3 and micrantha, Plumbago zeylanica, and Portulaca 4). Repeated H. velox hawkmoth outbreaks at oleracea (Table 3). NE Herald have caused stress to Pisonia trees and the defoliation of foliage (Smith and Pa- pacek 2004). It was recorded in 2006 and in Dieback of Pisonia grandis May 2007 that the larvae of H. velox had High populations of the soft scale insect Pul- caused approximately 72% defoliation (Free- vinaria urbicola and damage to P. grandis bairn 2006c,d, 2007). In November 2006 forest were first recorded at South-West Cor- G.N.B. (unpubl. data) also recorded Austra- inga Islet (SW Coringa) in 1991 (Donaldson lian native giant grasshopper (Valanga irregu- 1994, Smith and Papacek 2001a,b,c). Severe laris) grazing Pisonia foliage. It is important to defoliation by the larvae of the hawkmoth note that there was no dieback of Pisonia trees Hippotion velox was also observed on the P. directly linked to the Australian native insects grandis immediately before the soft scale out- (i.e., giant grasshopper and/or hawkmoth de- break (M. Hallam, pers. comm., 1997). Ac- foliation [G.N.B., unpubl. data; J.A.O., pers. cording to rainfall data presented in Figures obs., May 2007). 3 and 4, this high population of insects fol- In July 2001, biological control of scale lowed two to four ‘‘wet’’ periods of above- insects was implemented at NE Herald average rainfall. By 1994, up to 90% of the using the Australian native predatory ladybird trees were defoliated due to scale damage (Cryptolaemus montrouzieri) and three species (Donaldson 1994). According to P. O’Neill, of soft scale parasitoid wasps (Smith and J.A.O., and R. Elder (unpubl. data) and M. Papacek 2001b,c). In subsequent years, C. Hallam (pers. comm., 2007), during the 1997 montrouzieri and hawkmoth larvae egg parasi- surveys P. grandis dieback was estimated at toids were also released at NE Herald (Free- between 80% and 90%. Examination of cli- bairn 2006c,d, 2007). According to Freebairn mate data indicates that loss of Pisonia forests (2007), major losses of Pisonia dieback were from 1993 to 1998 occurred during a transi- avoided due to the effective biological control tion from a ‘‘wet’’ period to a ‘‘drought.’’ program of predatory ladybird releases and This infestation caused the loss of the entire the baiting of exotic ants (Tetramorium bicar- 10 ha of Pisonia forest at SW Coringa by inatum and Monomorium sp.). The exotic ants 2002 (Figure 6) (Smith et al. 2004). facilitate the spread of Pulvinaria urbicola Scale insects have also been detected on through active attending of the scale insects. North-East Herald Cay (NE Herald) since Nevertheless, during the prolonged drought 1994 (Donaldson 1994; P. O’Neill, J.A.O., period that has occurred since 2001 (Figures 82 PACIFIC SCIENCE . January 2010

TABLE 3 Terrestrial Plant Species Recorded at Coringa-Herald National Nature Reserve: 1960–2007 (Batianoff et al. 2009)

Islandsb

Life FAMILY Species Name Forma NEH SWH CI SWC SEM

AMARANTHACEAE Achyranthes aspera L. Hp X X X X X BORAGINACEAE Argusia argentea (L.f.) Heine ST X X X X X Cordia subcordata Lam. ST X — X X BRASSICACEAE Lepidium englerianum (Muschl.) Al-Shehbaz Ha X X X X X Ipomoea macrantha Roem. & Schult. Vp X X X X FABACEAE Canavalia rosea (Sw.) DC. Vp — — — — X GOODENIACEAE Scaevola taccada (Gaertn.) Roxb. ST E — — — — MALVACEAE Abutilon albescens Miq. S X X X X X Boerhavia albiflora Fosberg var. albiflora Hp X X X X X Boerhavia mutabilis R. Br. Hp X — — X X Pisonia grandis R. Br. T X — — E X OLACACEAE Ximenia americana L. ST E — — — — PLUMBAGINACEAE Plumbago zeylanica L. Hp — X X X X POACEAE Digitaria ctenantha (F. Muell.) Hughes Ha E — — — E Lepturus repens (G. Forst.) R. Br. Ha X X X X X Sporobolus virginicus (L.) Kunth Hp X X X — X Stenotaphrum micranthum (Desv.) C. E. Hubb. Ha X X X — X PORTULACACEAE Portulaca oleracea L. Ha/Hp X X X X X RHAMNACEAE Colubrina asiatica Brongn. S — — — — X ZYGOPHYLLACEAE Tribulus cistoides L. Ha/Hp X X X X X 12 families, 16 genera, 17 spp. (excluding 3 spp. 14 (þ3E) 12 12 12 (þ1E) 17 (þ1E) locally extinct)

Note: Status: X, recorded; E, presumed locally extinct. Nomenclature follows Bostock and Holland (2007). a Ha, annual/early maturing short-lived herb; Hp, perennial herb; Vp, perennial vine; S, shrub; ST, tall shrub/small tree (2–5 m); T, tree (>2 m). b NEH, NE Herald Cay; SWH, SW Herald Cay; CI, Chilcott Island; SWC, SW Coringa Islet; SEM, SE Magdelaine Cay.

3–5), some Pisonia dieback (1–2 ha) was re- original CHNNR of 40 ha (Batianoff et al. corded (Batianoff et al. 2009). The 2001– 2009). 2007 drought period has been the longest Other islands where P. urbicola infestations (Figure 5) and most intense continued rainfall of P. grandis have contributed to dieback in- deficit ever recorded (Figure 4). The com- clude Palmyra 1,680 km south of Ha- bined loss of P. grandis at SW Coringa and wai‘i, Rose Atoll in American , Bird NE Herald is estimated at 12 ha, 30% of its Island in the , and Tryon Island Climate and Vegetation Changes at Coringa-Herald . Batianoff et al. 83

Figure 6. Decline in Pisonia grandis cover at South-West Coringa Islet, 1991–2002, derived from M. Hallam (pers. comm., 2005). within the Capricornia Cays of the southern buildup during ‘‘La Nin˜ a’’ phases of ENSO, (Handler et al. 2007; A. with dieback occurring during and after pro- Kay, J.A.O., R. Elder, and K. Bell, unpubl. longed droughts. Extremes in climate vari- data; J.A.O., K. L. Bell, and R. J. Elder, un- ability have been suggested as an underlying publ. data; J.A.O., R. J. Elder, R. M. Charles, cause affecting the resilience of P. grandis in- J. R. Platten, and K. L. Bell, unpubl. data). dividuals, thus making them more susceptible Around 90% of the Pisonia forest at Tryon Is- to insect infestation (Greenslade 2008). How- land was lost between 1994 and 2005. Infesta- ever, this claim of P. grandis vulnerability to tions have also been recorded on Wilson and climate variability is somewhat negated by Heron islands within the Capricornia Cays natural resilience of P. grandis to its environ- from 2006 to 2007 (Freebairn 2006b; J.A.O., ment. This species is well adapted to seasonal unpubl. data; J.A.O., K. L. Bell, and R. J. drought conditions by its ability to be dor- Elder, unpubl. data). Damage to Wilson Is- mant (shed leaves) and store moisture in its land forest was prevented by use of ladybird trunk. The rapid deaths of Pisonia trees at predators (Cryptolaemus montrouzieri). The SW Coringa (Figure 7) may be due to a com- small Heron Island infestation of Pisonia rain bination of factors such as the increased insect forest was contained by pruning and remov- populations, as well as the increased moisture ing scale insect–affected material. Most of stress and brackishness of the freshwater lens the Capricornia Cays scale infestations are re- during the prolonged drought conditions and ported without any reference to climatic con- current temperature increases (Table 2). ditions (Freebairn 2006b). Rainfall records for The phenomenon of rapid insect popula- Heron Island (30 km southeast of Tryon Is- tion increases during wet periods and dieback land) show increased rainfall before the P. ur- during droughts has been reported from else- bicola outbreak at Heron Island and reduced where in northern Australia (White 1969). rainfall during the outbreak on Tryon Island Insect populations have also been shown to ( J.A.O., K. L. Bell, and R. J. Elder, unpubl. increase in abundance with temperature rises data). (Porter et al. 1991, Cannon 1998, Ayres and The scale insect increases at CHNNR Lombardero 2000, Bale et al. 2002). During have always followed periods of moisture drought conditions, freshwater lenses often 84 PACIFIC SCIENCE . January 2010

Figure 7. Analysis of scale insect (Pulvinaria urbicola) populations on Pisonia grandis leaves following release of pred- atory ladybirds (Cryptolaemus montrouzieri) at North-East Herald Cay, 2001–2007. (Source: Smith and Papacek 2001a,b and Freebairn 2007.)

become more brackish and/or undergo re- tendant ant Tetramorium bicarinatum (Ny- treat (White et al. 2007) thereby stressing lander) (Smith and Papacek 2001a). This plants that rely on freshwater lenses (Gessel facultative mutualism between scale and other and Walker 1992). The insect damage and exotic ant species has also been highlighted moisture stress could also have affected the for the P. grandis dieback at other locations soil nutrient uptake of Pisonia by reducing (i.e., Pheidole megacephala [Fabricius], Anoplo- the abundance of vesicular-arbuscular mycor- lepis gracilipes [Smith], and another exotic rhizal (VAM) fungi that inhabit P. grandis brown ant, Monomorium sp. [Handler et al. roots (Ashford and Allaway 1982, Chambers 2007; A. Kay, J.A.O., R. Elder, and K. Bell, et al. 2005). unpubl. data; J.A.O., unpubl. data; J.A.O., Pulvinaria urbicola is a soft scale that is na- K. L. Bell, and R. J. Elder, unpubl. data; tive to the West Indies but is exotic to Austra- J.A.O., R. J. Elder, R. M. Charles, J. R. Plat- lia (Smith and Papacek 2001a, Handler et al. ten, and K. L. Bell, unpubl. data]). Scale in- 2007; A. Kay, J.A.O., R. Elder, and K. Bell, sects together with attendant ants have been unpubl. data). It is assumed that this pest has able to rapidly infest most of the Pisonia for- invaded CHNNR only recently because the est including other species that were more species had not been reported damaging Piso- resilient to the scale’s damage (Smith and Pa- nia trees before the early 1990s. Most in- pacek 2001a,b,c). festations at CHNNR were recorded in The question remains as to why scale in- relation to higher numbers of the exotic at- sect outbreaks have occurred at so many loca- Climate and Vegetation Changes at Coringa-Herald . Batianoff et al. 85 tions in the Pacific and Indian oceans at more by establishing new populations (Batianoff or less the same time. The reasons for current et al. 2009). The May 2007 and October/ Pisonia dieback are complex. The increased November 2007 surveys showed large areas winter temperatures may have resulted in the of dead Argusia, at the same time that some earlier breeding onset of scale insect genera- new colonizations were taking place along tions during favorable wet seasons. However, the seaward margins. During the last 20 yr, the main reason for current Pisonia dieback the Argusia plant community has undergone seems to be the combination of climatic fac- cyclic dieback of older stands followed by tors that favor native and exotic insect herbi- some recovery as well as establishment of vores, together with the natural vulnerability new seedlings along the seaward margins. of Pisonia to scale insect damage. Argusia argentea is listed as a threatened species on the IUCN Red List (IUCN 2008). Substantial losses of stands at Dieback of Argusia argentea Argusia CHNNR should be regarded as a threatening Argusia argentea is a wind-shear tolerant, ha- process to coral cay ecosystems. The over- lophytic species that readily colonizes the story canopy provides key primary nesting seaward margins of coral cays. It is able to habitat for many arboreal-nesting seabirds tolerate salt spray and brackish water table such as the Red-footed Booby, Great and conditions (Batianoff et al. 2009). The A. ar- Lesser Frigatebirds, and Common and Black gentea community occurs on all of the vege- Noddies (Batianoff 2001a). It is also the pre- tated cays at CHNNR (Table 3). During the ferred shelter for ground-nesting birds such 2006–2007 surveys, up to 50% of A. argentea as the Red-tailed Tropicbird and the Brown stands were dead or showing symptoms of Booby. On smaller cays, it is the only woody dieback (Batianoff et al. 2009). Dieback and plant providing ‘‘arboreal’’ nesting habitat for tree deaths were most pronounced along seabirds. As in the case of Pisonia grandis loss, landward margins within the older stands. we have observed that ground cover species The estimated proportion of trees affected take the place of Argusia vegetation soon after by dieback were South-East Magdelaine Cay the dieback. Along the seaward margins the (SE Magdalaine) (30–50%), NE Herald (25– most common species replacing Argusia is 30%), SW Coringa (10–20%), South-West Sporobolus virginicus. The landward or the in- Herald Cay (SW Herald) (10–15%), and terior open areas with Argusia dieback are Chilcott Island (5–10%). Some basal re- frequently invaded by ground cover species sprouting was observed within the dieback such as Abutilon albescens, Achyranthes aspera, populations. However, on average, only 3– Ipomoea macrantha, and Portulaca oleracea. 5% of the populations was showing any re- The extent of Argusia dieback was variable covery (Batianoff et al. 2009). due to the configuration and size of each is- Dieback of A. argentea was first reported land. The larger islands (i.e., NE Herald, by Donaldson (1994) at NE Herald. He sug- SE Magdelaine, and SW Coringa) have gested that a combination of an unknown greater areas of mature A. argentea stands ex- fungal disease and lower rainfall had caused tended inshore. As a result, the dieback areas the dieback. These observations were made of Argusia were also greater. No symptoms of toward the end of a 5- to 6-yr drought pests or pathogens were observed during the (Figures 2 and 3), and moisture stress was 2006–2007 surveys, though susceptibility to undoubtedly a key element that caused die- heliotrope moth larvae has been reported on back in mature stands of A. argentea. During other Pacific islands (Manner and Elevitch a survey in July 1997, Batianoff (2001b) 2006). We postulate that A. argentea is observed Argusia communities to be in a rela- adapted for warmer climatic conditions and tively healthy state. Oblique aerial photogra- periodic 2- to 4-yr droughts. However, ma- phy (2001) of NE Herald indicates that ture Argusia plants along landward margins some A. argentea stands along landward mar- are vulnerable to the current prolonged gins had recovered from the 1994 dieback drought conditions. 86 PACIFIC SCIENCE . January 2010

Dieback of Cordia subcordata to extensive clearing for timber and devel- opment throughout its global distribution Well-developed stands of Cordia subcordata (IUCN 2008). Our current interpretation of are recorded on the larger cays within forest defoliation and/or dieback during dry CHNNR (NE Herald and SE Magdelaine). periods requires caution. Cordia subcordata is Smaller populations of C. subcordata occur at capable of strong recovery during wet peri- SW Coringa and Chilcott Island. The well- ods through vegetative regrowth. As a result, developed, dense Cordia thickets are difficult some dry leafless stems that may have been for larger seabirds and humans to traverse recorded as dead due to dieback may actually (Batianoff et al. 2009). Leafless conditions of recover by root sprouting following suitable Cordia were first reported by J. Hicks (un- rainfall events. publ. data) in December 1983 and October 1984 at NE Herald. During the 1994 survey Dieback of Other Vegetation of NE Herald, Donaldson (1994) recorded Cordia defoliation by grasshoppers and/or Ximenia americana was first recorded at NE hawkmoth larvae. In June 1997, a wet period Herald as a small tree in December 1983 (Figures 2, 3), Batianoff (2001b) reported (Du Puy and Telford 1993). Ten individuals healthy stands of C. subcordata at NE Herald. of different ages were recorded at the same His descriptions indicated full recovery of location in June 1997 (Batianoff 2001a). Dur- Cordia stands from the stressful periods re- ing the 2006–2007 surveys, it was observed ported by J. Hicks (unpubl. data) and Do- that the entire X. americana population had naldson (1994). died out (Table 3). The loss of X. americana Insect herbivory of C. subcordata was also from NE Herald is not attributed to scale recorded at NE Herald by Smith and Papa- insect damage. On Tryon Island, Ximenia cek (2001a) and Freebairn (2006a,c,d, 2007). plants were not observed to be damaged They reported damage caused by the larvae by scale insects (G.N.B., unpubl. data). The of the noctuid moth Armactica columbina most likely reason for Ximenia dieback is the (Walker). Complete defoliation by the same prolonged droughts (Batianoff et al. 2009). species was observed by Freebairn (2006c) However, X. americana forms parasitic rela- during the May 2006 survey of NE Herald. tionships with the roots of nearby host plants During our November–December 2006 sur- (Male´cot and Nickrent 2008). As a result, the vey, more than half of the total C. subcordata loss of the host plants such as Pisonia during areas showed symptoms of dieback, with ex- the drought most likely contributed to local tensive leaf damage by the noctuid moths extinctions of X. americana. and/or the giant grasshopper Valanga irregu- Three annual or short-lived grass species laris (Walker). About 15% of plants were re- in the last decade have shown reduced cov- covering vegetatively via basal shoots. By May erage and/or local extinction: Digitaria cte- 2007, C. subcordata plants showed preferential nantha, Lepturus repens, and Stenotaphrum defoliation by noctuid moth larvae and grass- micranthum (Table 3). Specimens of Digita- hoppers, with >90% of the Cordia population ria ctenantha were collected at SE Mag- leafless. The symptoms in dieback stands delaine in May 1984 and October 1987 were more evident (>70% of total area), (Telford 1993). It was also collected at NE with less than 10% recovery via vegetative Herald during June 1997 (Batianoff 2001a). basal shoots. However, during the 2006–2007 surveys, we It should be noted that the soft scale insect were not able to find D. ctenantha at either Pulvinaria urbicola appears to avoid Cordia island. It is now considered locally extinct plants. For example, at SW Coringa two from CHNNR (Batianoff et al. 2009). small Cordia stands remain standing after the Decline in grassy ground cover in the inte- loss of the entire Pisonia forest from 1991 to rior areas at NE Herald was estimated at 20– 2001 (Batianoff et al. 2009). Cordia is listed 30% in June 1997 but reduced to 5–10% in as threatened on the IUCN Red List due 2006–2007. This moderate reduction of Climate and Vegetation Changes at Coringa-Herald . Batianoff et al. 87 ground cover of Lepturus repens and Steno- activities have also facilitated the introduction taphrum micranthum occurred under the Abu- of insect pests, causing or exacerbating major tilon albescens overstory. At SW Herald, the wildlife changes in this region. The exotic ant dominant grassy cover in the interior was es- Tetramorium bicarinatum is native to South- timated at 50–70% in October 1984 by J. east Asia (Shattuck and Barnett 2001). Ac- Hicks (unpubl. data) and T. Ayling (pers. cording to Greenslade (2008), this ant and comm., 2007) but was reduced to 10–15% Pulvinaria urbicola may have been present in by 2006–2007 (Batianoff et al. 2009). The the study area in low numbers for many years. loss of grasses was associated with an expan- We have no documented knowledge as to sion of A. albescens open-heath. These major when, and how, exotic pest insects arrived in changes mainly affected short-lived grasses, CHNNR. Pulvinaria urbicola utilizes a broad because coverage of the perennial grass Spor- spectrum of plant species, and it is common obolus virginicus remained unaffected at NE in Queensland and other regions (Freebairn and SW Herald. 2007; J.A.O., K. L. Bell, and R. J. Elder, un- The reasons for reduction and/or loss of publ. data). According to Smith and Papacek short-lived grass species in the interior areas (2001a), this scale insect most likely arrived during droughts is difficult to explain. Loss from the mainland on fruits and/or vegetables of soil bank due to the inability to repro- consumed by visitors to CHNNR and/or duce during moisture stress periods is offered Willis Island. Once established locally, the as one of the major reasons. However, at NE scale insects are probably successfully travers- Herald during the 2006–2007 surveys, many ing the shorter distances required for island Lepturus repens were observed being hopping via transportation by seabirds and/ harvested by ants (Tetramorium bicarinatum). or wind. The recent arrival of the exotic ant Hence, the decline in annual grass species at Pheidole megacephala at Willis Island coincided CHNNR is potentially being caused by ex- with the expansion of the Meteorological Sta- otic ants removing seeds and thus reducing tion facilities. We speculate that arrival of T. the soil seed bank. bicarinatum in CHNNR was also facilitated by human activities, such as the use of old contaminated camping equipment on NE Management Implications Herald Cay (Greenslade 2008). Insect pest in- Coral cay ecosystems are resilient to climatic troduction by rafting on floating materials is disturbances (Batianoff 2001b, Turner and also a possibility. Batianoff 2007). Continuing sediment pro- Human activities, combined with current duction and additional accumulation of sand climate-change conditions, are already having most likely negate some of the predicted ef- a major impact on the day-to-day conserva- fects of sea immersion of low cays. During tion management of CHNNR. To maintain the current climate change, we require local biodiversity, wildlife habitats, and ecosystem knowledge for adaptive management (Turner function in CHNNR, Batianoff et al. (2009) and Batianoff 2007). The conservation au- and Greenslade (2008) have listed several thorities managing low islands should prepare biosecurity procedures designed to minimize for two scenarios: (1) major reduction in size, the risk of further pest introduction. Batian- and losses, of low islands; or (2) increased off et al. (2009) recommended corrective in- sizes of the older surviving cays and forma- terference and restoration of some habitats tion of new coral cays. to facilitate desirable ecosystems after es- Loss of large areas of vegetation due to tablishment of pest populations at conser- dieback, particularly the P. grandis forests in vation reserves. For example, biological CHNNR, indicates that major environmental control programs to control scale populations changes have already occurred. We postulate using the predatory ladybird Cryptolaemus that severity of dieback is due to current montrouzieri and parasitoid wasps have been climatic trends of prolonged droughts and relatively successful (Smith et al. 2004, Free- temperature increases. Unintentional human bairn 2007; J.A.O., unpubl. data; J.A.O., K. L. 88 PACIFIC SCIENCE . January 2010

Bell, and R. J. Elder, unpubl. data). These ef- argentea also facilitates colonization and stabi- fective control measures were used on NE lization of coral cay beaches. Herald and Wilson Island. The release of Overall, CHNNR vegetation shows resil- ladybird predators is usually done in conjunc- ience to variable and harsh seasonal climatic tion with ant baiting. conditions and is capable of withstanding a If rain forest diversity that is functional for wide range of temperatures, droughts, cy- wildlife such as seabirds is to be maintained clones, and saltwater intrusions. These and/or restored at CHNNR, then manage- relatively simple communities are ideal eco- ment interventions may be necessary to re- systems in which changes can be rapidly as- store former P. grandis rain forest areas at sessed. Despite current climate trends, the SW Coringa. Hand-in-hand with this vegeta- rates of vegetation change and species turn- tion management restoration is the need for over are also dependent on individual coral continued control of populations of scale in- cay characteristics and human activities. The sects and exotic ants. The recovery of P. decline of some important plant species that grandis by planting stem cuttings following provide a high level of functional diversity is scale insect damage has been successfully im- a challenge for conservation management of plemented at Tryon Island (Cruise et al. CHNNR. Cooperative conservation work at 2006; J.A.O., unpubl. data; J.A.O. and Brushe, Willis Island is an important step for wildlife unpubl. data, 2007 and 2008). Once a few management at CHNNR as well as other patches of P. grandis have been reestablished, cays in the Coral Sea Islands Territory. the natural ability of vegetative growth by stem layering is considered sufficient for its acknowledgments survival and spread. We also advise that any future planting of P. grandis should coin- We are grateful to Neil Gemmell and Astrida cide with the ‘‘wet’’ seasons to improve the Mednis for their leadership and the assistance chances of reestablishment. Finally, the anal- in preparation of earlier survey reports. Mark yses of scale insect population increases at Hallam (formerly of the Department of the CHNNR indicate that it is most important Environment, Water, Heritage, and the Arts) to check for plague scale damage immediately is particularly acknowledged for his generous after a ‘‘La Nin˜ a’’ phase of ENSO. sharing of local knowledge. The Director of the Queensland Herbarium, Gordon Guy- conclusions mer, is acknowledged for his guidance and support. Critical comments on early drafts The reasons for the current dieback of a wide were provided by Herbarium staff: Paul For- range of plants at CHNNR are complex. ster and Rod Fensham. Most of the wildlife changes reported here are linked to current climate trends includ- Literature Cited ing moderate rises in temperature and drought frequency and intensity. Uninten- Ashford, A. E., and W. G. Allaway. 1982. A tional spreading of exotic insect species sheathing mycorrhiza on Pisonia grandis through human activities, combined with cli- R.Br. (Nyctaginaceae) with development mate change, has contributed to unforseen of transfer cells rather than a Hartig net. changes in vegetation. The loss of the Pisonia New Phytol. 90:511–519. grandis rain forest is due to damage by scale Ayres, M. P., and M. J. Lombardero. 2000. insects and their attendant exotic ants. The Assessing the consequences of global reasons for the reduction of short-lived grass change for forest disturbance from herbi- species requires further investigation. Argusia vores and pathogens. Sci. Total Environ. argentea dieback has resulted in the major loss 262:263–286. of the salt spray/windbreak, as well as nesting Baker, B., M. Double, R. Gales, M. Holds- and shelter habitats for seabirds and other worth, and M. R. Hallam. 2006. Seabird . The protective fringe formed by A. monitoring program-Coral Sea Island Climate and Vegetation Changes at Coringa-Herald . Batianoff et al. 89

Territory: Report on 2006 field season and ience to environmental stressors, includ- update of Herald Cays longitudinal data- ing climate change and pests. Queensland sets for the period 1999–2006. Report to Herbarium, Environmental Protection the Department of the Environment and Agency, Brisbane. Heritage, . Bostock, P. B., and A. E. Holland, eds. 2007. Baker, B., M. Holdsworth, L. Finley, and M. Census of the Queensland flora 2007. Double. 2008. Seabird monitoring study at Queensland Herbarium, Environmental Coringa-Herald National Nature Reserve. Protection Agency, Brisbane. Report to the Department of the Environ- Bureau of Meteorology. 2008a. Climate data, ment, Water, Heritage and the Arts, Can- http://www.bom.gov.au/climate/averages berra. (accessed 31 July 2008). Bale, J. S., G. J. Masters, I. D. Hodkinson, C. ———. 2008b. Tropical cyclone warning Awmack, T. M. Bezemer, V. K. Brown, J. services: Tropical cyclone information for Butterfield, A. Buse, J. C. Coulson, J. Far- Australia and , rar, J. E. G. Good, R. Harrington, S. Hart- http://www.bom.gov.au/cgi-bin/silo/cyclones ley, T. H. Jones, R. L. Lindroth, M. C. .cgi. (accessed 31 July 2008). Press, I. Symrnioudis, A. D. Watt, and Cai, W., S. Crimp, K. McInnes, B. Hunt, R. J. B. Whittaker. 2002. Herbivory in global Suppiah, M. Collier, T. Elliott, K. Hen- climate change research: Direct effects of nessy, R. J. Jones, C. Page, and P. Whet- rising temperature on insect herbivores. ton. 2003. Climate change in Queensland Glob. Change Biol. 8:1–16. under enhanced greenhouse conditions. Batianoff, G. N. 2001a. Observation of trop- Final report 2002–2003. CSIRO Atmo- ical seabird breeding sites and utilisation spheric Research, Aspendale, . of seashore plants on North-East Cay Cannon, R. J. C. 1998. The implications (Herald Cays), Coral Sea. Pages 11–20 in of predicted climate change for insect L. Comben, ed. Herald Cays scientific pests in the UK, with emphasis on non- study report. Royal Geographic Society of indigenous species. Glob. Change Biol. Queensland, Brisbane. 4:785–796. ———. 2001b. Terrestrial flora and vegeta- Chambers, S. M., C. J. Hitchcock, and tion of North-East Cay (Herald Cays), J. W. G. Cairney. 2005. Ectomycorrhizal Coral Sea Islands Territory, Australia. mycobionts of Pisonia grandis on coral Pages 21–31 in L. Comben, ed. Herald cays in the Capricorn-Bunker Group, Cays scientific study report. Royal Geo- Great Barrier Reef, Australia. Mycol. Res. graphical Society of Queensland, Brisbane. 109:1105–1111. Batianoff, G. N., and N. J. Cornelius. 2005. Cruise, J., J. A. Olds, and R. Melzer. 2006. Birds of Raine Island: Population trends, Tryon Island restoration: Project brief. breeding behaviour and nesting habitats. Pest arrest in central Queensland. Queens- Proc. R. Soc. Queensl. 112:1–29. land Parks and Wildlife Service, Environ- Batianoff, G. N., and G. C. Naylor. 2007. As- mental Protection Agency, Rockhampton. sessment of Pisonia grandis forest condition Donaldson, S. R. 1994. Preliminary report on and ecology at Coringa-Herald National April 1994 Coral Sea National Nature Re- Nature Reserve, Coral Sea. Report on the serve Patrol. Report to Environment Aus- field survey of North-East Herald Cay and tralia, Canberra. South-West Herald Cay: 27th November– Du Puy, D. J., and I. R. H. Telford. 1993. 6th December 2006. Report to the De- Olacaceae. Pages 255–256 in ABRS, Flora partment of the Environment and Water of Australia 50: Oceanic islands 2. Austra- Resources, Canberra. lian Government Publishing Service, Can- Batianoff, G. N., G. C. Naylor, and H. A. berra. Dillewaard. 2009. Coringa-Herald Na- Environment Australia. 2001. Coringa- tional Nature Reserve: Assessment of Herald National Nature Reserve and Li- vegetation conditions, ecology and resil- hou Reef National Nature Reserve man- 90 PACIFIC SCIENCE . January 2010

agement plan. Environment Australia, Greenslade, P., and R. Farrow. 2007. Report Canberra. on survey and collection of the inverte- Farrow, R. A. 1984. Detection of transoce- brate fauna at Coringa-Herald National anic migration of insects to a remote island Nature Reserve, May 13–19, 2007. Report in the Coral Sea, Willis Island. Aust. J. to the Department of the Environment Ecol. 9:253–272. and Water Resources, Canberra. Fensham, R. J., R. J. Fairfax, and D. P. Ward. Handler, A. T., D. S. Gruner, W. P. Haines, 2009. Drought-induced tree death in sav- M. W. Lange, and K. Y. Kaneshiro. 2007. anna. Glob. Change Biol. 15:380–387. surveys on , Line Foley, J. C. 1957. Droughts in Australia: Re- Islands, and insights into the decline of the view of records from earliest years of set- native tree Pisonia grandis (Nyctaginaceae). tlement to 1955. Bulletin No. 47, Bureau Pac. Sci. 61:485–502. of Meteorology, Melbourne. Heatwole, H. 1979. Report on fauna and Freebairn, C. G. 2006a. Pulvinaria urbicola on flora of the lands of the Coral Sea Islands Pisonia grandis in the Coringa-Herald Na- Territory. Report to the Australian Na- tional Nature Reserve: July 2004 and Au- tional Parks and Wildlife Service, Can- gust 2005. Report to the Department of berra. the Environment and Heritage, Canberra. Hicks, J., and M. Hinchey. 1984. Coringa- ———. 2006b. Report on a visit to the Herald National Nature Reserves field Capricorn-Bunker islands, 7–11 August trip, 7–12 December 1983. Report to the 2006: Pulvinaria urbicola scale and panda- Australian National Parks and Wildlife nus dieback investigations. Report to the Service, Canberra. Environmental Protection Agency, Rock- Hinchey, M. D., and T. Stokes. 1987. Coral hampton. Sea National Nature Reserves: Report on ———. 2006c. The scale insect Pulvinaria ur- patrol to Coringa Islet, Nellie Cay and bicola and the hawkmoth Hippotion velox on Georgina Cay. Report to the Australian Pisonia grandis on NE Herald Islet in the National Parks and Wildlife Service, Can- Coringa-Herald National Nature Reserve: berra. May 2006. Report to the Department of Hughes, L. 2003. Climate change and Austra- the Environment and Heritage, Canberra. lia: Trends, projections and impacts. Aus- ———. 2006d. The scale insect Pulvinaria tral. Ecol. 28:423–443. urbicola and the hawkmoth Hippotion velox Intergovernmental Panel on Climate Change. on Pisonia grandis on NE Herald Islet, 2007. Climate change 2007: The physical Coringa-Herald National Nature Reserve: science basis. Contribution of Working December 2006. Report to the Depart- Group I to the Fourth Assessment Report ment of the Environment and Heritage, of the IPCC, edited by S. Solomon, D. Canberra. Qin, M. Manning, Z. Chen, M. Marquis, ———. 2007. The scale insect Pulvinaria ur- K. B. Avery, M. Tignor, and H. R. Miller. bicola and the hawkmoth Hippotion velox Cambridge University Press, Cambridge. on Pisonia grandis on NE Herald Islet, IUCN. 2008. 2008 Red List of threatened Coringa-Herald National Nature Reserve: species, http://www.iucnredlist.org (ac- May 2007. Report to the Department of cessed 2 November 2008). the Environment and Heritage, Canberra. Johnson, J. E., and P. A. Marshall, eds. 2007. Gessell, S. P., and R. B. Walker. 1992. Climate change and the Great Barrier Studies of soils and plants in northern Mar- Reef: A vulnerability assessment. Great shall Islands. Atoll Res. Bull. 359:1–70. Barrier Reef Marine Park Authority and Greenslade, P. 2008. Climate variability, bio- Australian Greenhouse Office, Australia. logical control and an insect pest outbreak Kepler, A. K., and C. B. Kepler. 1994. Part I. on Australia’s Coral Sea islets: Lessons for History, physiography, botany, and isle de- invertebrate conservation. J. Insect Con- scriptions. Atoll Res. Bull. 397:1–225. serv. 12:333–362. Lough, J. M. 2007. Climate and climate Climate and Vegetation Changes at Coringa-Herald . Batianoff et al. 91

change on the Great Barrier Reef. Pages www.environment.gov.au/coasts/mpa/ 15–50 in J. E. Johnson and P. A. Marshall, publications/pubs/coringa-pest-scale-2.pdf eds. Climate change and the Great Barrier ———. 2001c. Report on visit to the Reef: A vulnerability assessment. Great Coringa-Herald National Nature Reserve, Barrier Reef Marine Park Authority and 30 July–10 August 2001, with regard to Australian Greenhouse Office, Australia. the releasing of parasitoids and ladybird Male´cot, V., and D. L. Nickrent. 2008. Mo- predators of the pest scale Pulvinaria urbi- lecular phylogenetic relationships of Ola- cola on Pisonia grandis. Report to Envi- caceae and related Santalales. Syst. Bot. ronment Australia, Canberra. Available at 33:97–106. www.environment.gov.au/coasts/mpa/ Manner, H. I., and C. R. Elevitch. 2006. publications/pubs/coringa-pest-scale-2.pdf Tournefortia argentea (tree heliotrope). ———. 2004. Report on the levels of Pulvi- Permanent agriculture resources 2006, naria urbicola (and its natural enemies) http://www.traditionaltree.org (accessed and hawkmoths on Pisonia grandis in the 31 January 2008). Coringa-Herald National Nature Reserve, Mueller-Dombois, D., and F. R. Fosberg. 2–7 April 2004. Report to Environment 1998. Vegetation of the tropical Pacific is- Australia, Canberra. Available at www lands. Springer-Verlag, New York. .environment.gov.au/coasts/mpa/publications/ Myers, M., and J. Kent, eds. 2005. The new pubs/coringa-pest-scale-2.pdf Gaia atlas of planet management. Gaia Smith, D., D. Papacek, M. Hallam, and J. Books, London. Smith. 2004. Biological control of Pulvina- Porter, J. H., M. L. Parry, and T. R. Carter. ria urbicola (Cockerell) (Homoptera: Coc- 1991. The potential effects of climatic cidae) in a Pisonia grandis forest on North- change on agricultural insect pests. Agric. East Herald Cay in the Coral Sea. Gen. For. Meteorol. 57:221–240. Appl. Entomol. 33:61–68. Royal Geographical Society of Queensland. Smith, J. M. B. 1994. Patterns of disseminule 2001. Herald Cays scientific study report, dispersal by drift in the north-west Coral Vol 6. Royal Geographical Society of Sea. N. Z. J. Bot. 32:453–461. Queensland, Fortitude Valley. Specht, R. L., and A. Specht. 1999. Australian Shattuck, S. O., and N. J. Barnett. 2001. Aus- plant communities: Dynamics of structure, tralian ants online: The guide to the Aus- growth and biodiversity. Oxford Univer- tralian ant fauna. CSIRO 2001, http:// sity Press, Melbourne. www.ento.csiro.au/science/ants/myrmicinae/ Stoddart, D. R., and R. P. D. Walsh. 1992. tetramorium/tetramorium_tax_cat.htm Environmental variability and environ- (accessed October 2008). mental extremes as factors in the island Smith, D., and D. Papacek. 2001a. Report on ecosystem. Atoll Res. Bull. 356:1–71. the levels of the scale insect Pulvinaria ur- Suppiah, R., D. Collins, and P. Della-Marta. bicola and its natural enemies on Pisonia 2001. Observed changes in Australian cli- grandis in the Coringa-Herald National mate. CSIRO Atmospheric Research and Nature Reserve 16–23 March 2001. Re- Bureau of Meteorology, Canberra. port to Environment Australia, Canberra. Telford, I. R. H. 1993. Coral Sea Islands Available at www.environment.gov.au/ Territory. 50:47–53. coasts/mpa/publications/pubs/coringa-pest- Turner, M., and G. N. Batianoff. 2007. Vul- scale-2.pdf nerability of island flora and fauna in the ———. 2001b. Report on visit to the Great Barrier Reef to climate change. Coringa-Herald National Nature Reserve, Pages 621–666 in J. E. Johnson and P. A. 17–21 December 2001, with regard to Marshall, eds. Climate change and the the releasing of parasitoids and ladybird Great Barrier Reef: A vulnerability assess- predators of the pest scale Pulvinaria urbi- ment. Great Barrier Reef Marine Park Au- cola on Pisonia grandis. Report to Environ- thority and Australian Greenhouse Office, ment Australia, Canberra. Available at Australia. 92 PACIFIC SCIENCE . January 2010

Walker, B., and D. Salt. 2006. Resilience fluences on groundwater in low . Va- thinking: Sustaining ecosystems and peo- dose Zone J. 6:581–590. ple in a changing environment. Island White, T. C. R. 1969. An index to measure Press, Washington. weather-induced stress of trees associated White, I., T. Falkland, T. Metutera, E. with outbreaks of psyllids in Australia. Metai, M. Overmars, P. Perez, and A. Ecology 50:905–909. Dray. 2007. Climatic and human in-