ECOSYSTEM ECOLOGY

Matthew J. Wooller Æ Beverly J. Johnson

Andrew Wilkie Æ Marilyn L. Fogel

Stable isotope characteristics across narrow savanna / woodlandecotones in Wolfe Creek Meteorite Crater, Western Australia

Received: 4 November 2004 / Accepted: 14 March 2005 / Published online: 26 May 2005� Springer-Verlag 2005

Abstract The stable isotopic composition (d13C) of sed-iments from lakes are frequently analyzed to reconstructthe proportion of the regional vegetation that used ei-ther the C3 or C4 photosynthetic pathways, often with-out conducting a detailed survey of the current localvegetation. We performed a study on the modern vege-tation composition within the Wolfe Creek MeteoriteCrater to complement our future paleoecological inves-tigation of the crater. A bull’s-eye pattern exists whereC4 grasses dominate an outer ring and salt tolerantspecies, including shrubs, herbs, chenopods, and halo-phytic algae, dominate the inner pan of the crater. Theecotone between the inner and outer zones is narrow andoccupied by tall (>7 m) Acacia ampliceps, with some C4

grasses in the understory. Along with the highest watertable and most saline soils the center of the crater has C3

plants present with the highest d13C and d15N values.The range of d13C and d15N values from the analysis ofsurface soil organic matter (OM) was much smallercompared with the range of values from plant materialsimplying that either: (1) the current plant OM has notyet been integrated into the soils, or (2) processes withinthe soil have acted to homogenize isotopic variabilitywithin the crater. The application of a two end member

mixing model to calculate %C4 and %C3 biomass fromthe d13C of surface soil OM was complicated by: (1) thecrater containing both a dry habitat with C4 grasses anda central pan with C4 halophytic plants and, (2) the largevariation in the d13C of the plants and soil OM.

Keywords Carbon Æ Nitrogen Æ C3 Æ C4 Æ Plants

Introduction

Changes in environmental conditions, including theconcentration of atmospheric CO2, disturbance, tem-perature, aridity, and salinity, can influence the com-petitive balance between plants using the C3 and C4

photosynthetic pathways (Ehleringer et al. 1997; Tieszen1991). C3 and C4 plants possess diagnostic stable carbonisotope ratios (d13C&) (Deines 1980) where C3 plants(most herbs and woody shrubs) are characterized byd13C values averaging �27& (�21 to �35&) and C4

plants average �12& (�10 to �14&) (Ehleringer 1991).Variations within C3 plants can result from a number offactors including canopy effects and moisture stress ei-ther driven by salinity or aridity (O’Leary 1988; Lin andSternberg 1992). The d13C values of sedimentary organicmatter (OM) in tropical and sub-tropical lakes are oftenused to reconstruct the past regional composition of C3

and C4 plants in lake catchments (e.g., Ficken et al.2002; Wooller et al. 2003a; Mora et al. 2002). Logisticalor financial constraints can sometimes prevent detailedsurveys of vegetation being considered for paleoecolog-ical research. In these instances regional or globalaverage d13C values for C3 and C4 plants have to be usedto interpret sedimentary d13C values.

The purpose of this study was to examine thevegetation distribution and d13C variation at a localscale across the Wolfe Creek Meteorite Crater(WCMC), Western Australia in an effort to charac-terize modern plant inputs into the sedimentaryrecord. The WCMC is one of the sites we are using to

Communicated by Lawrence Flanagan

M. J. Wooller (&) Æ M. L. FogelGeophysical Laboratory, Carnegie Institution of Washington,5152 Broad Branch Road NW,Washington DC, 20015-1305, USAE-mail: ffmjw@uaf.eduTel.: +1-907-4746738Fax: +1-907-4747979

B. J. Johnson Æ A. WilkieDepartment of Geology,Bates College, Lewiston, ME 04240, USA

M. J. WoollerAlaska Stable Isotope Facility,Water and Environmental Research Center and Schoolof Fisheries and Ocean Sciences,University of Alaska Fairbanks,Fairbanks, AK 99775, USA

Oecologia (2005) 145: 100–112DOI 10.1007/s00442-005-0105-5

reconstruct the past environments of Australia usingmultiple lines of evidence including d13C of OM.Considerable variability in d13C of OM from soils hasbeen demonstrated in Northern Australia at the re-gional and biome level (Bird and Pousai 1997). Adetailed local survey of the d13C variation in organiccomponents at a site being considered for paleoeco-logical investigation is valuable so as to criticallyinterpret d13C from sediments. We hypothesized thatthe stable isotopic composition of the soil OM (SOM)from the WCMC should reflect the modern vegetationcomposition within the crater, a prerequisite forpaleoecological interpretations of d13C analyses ofsediments. We hypothesized that the vegetation dis-tribution is related to evapotranspiration, soil mois-ture, and salinity. This hypothesis originated from ourinitial observations of the site, which showed that soilin the central part of the WCMC was encrusted withgypsum and was noticeably moist compared with therest of the soils in the crater. Both soil moisture andsalinity are known to influence the d13C of plants (e.g.,O’Leary 1988; Lin and Sternberg 1992). Quadratanalyses were performed to quantify the percent C3

and C4 plant cover. The d13C of plants and soils fromwithin the WCMC were determined to examine whe-ther the local C3 and C4 plant distribution was rep-resented in the surface soils. The d15N values of plantsand soils were also determined to investigate themagnitude of variation in the vegetation, which can bean effective marker of the nutrient status in a habitatthat can subsequently influence vegetation composi-tion, distribution, and structure (e.g., Evans 2001;Robinson 2001; McKee et al. 2002; Wooller et al.2003a, b; Jones et al. 2004). Soil-moisture and salinityof the groundwater, which are also known to influencethe d13C of plants (e.g., Lin and Sternberg 1992;Tieszen 1991; Archibold 1995) were also determined.These findings will subsequently aid interpretation ofd13C measurements of total organic carbon (TOC)preserved in a �10 m auger taken from the center ofthe WCMC (Wooller et al., in preparation).

Materials and methods

Study site

The WCMC (longitude 19�10¢E and latitude 127�47¢S),located south of Halls creek off of the Great NorthernHighway between the Tanami Desert to the east andthe Great Sandy Desert to the west, was discovered andnamed by Reeves and party in 1947 (Reeves andChalmers 1948). In 1948, the Australian Bureau ofMineral Resources (BMR) carried out the first detailedgeological investigation of the feature (Guppy andMatheson 1950) and attributed it to a meteoric impact,which was subsequently confirmed by others (Cassidy1954; LaPaz 1954; McCall 1965). Ratios of 36Cl/10Beand 41Ca/36Cl from an iron meteorite fragment

from the crater give an age of 300 ka for the crater(Shoemaker et al. 1990).

The WCMC is one of the largest and best-preservedimpact craters on Earth and is now a National Reservemanaged by the Western Australian Department ofConservation and Land Management (CALM). Thecrater has a mean diameter of approximately 880 m anda rim height of about 30 m above the surrounding plain.At the base of the steep inner walls, there is an abruptchange of slope to a gently sloping sand apron about280-m wide that is primarily covered in grasses. Theapron falls about 6 m to an extremely flat inner floorprimarily covered with trees and shrubs. The craterforms a topographically closed depression, but becauseof its very small catchment area and its position in thearid zone it cannot form a surface-water-fed lake(Bowler 1981, 1986) and the crater hydrology is domi-nated by groundwater. Subsequently, there is no year-round lake and standing water in the crater consists ofonly a few isolated pools (Fig. 1).

The climate of the area is strongly influenced by theAustralian monsoon during the summer months(December through March) and penetration of the InterTropical Convergence Zone (ITCZ) from the north,which brings �500 mm of precipitation annually.Evaporative water loss from the site is highest during themonths of September through January (e.g., averageDecember evaporation=300–350 mm) with mean an-nual evaporation �3,400 mm (Commonwealth Bureauof Meteorology 2003), which is evident from a concen-tration of gypsum forming a crust on the surface of thesoil towards the center of the crater. In July 2001,the water table was within �50 cm of the soil surface inthe center of the crater, and consequently, freestandingwater was present in isolated pools and dissolution pitstowards the center of the crater during the driest ofmonths.

Vegetation survey

Five areas were selected at the WCMC area in July2001: (1) the area immediately adjacent to and outsideof the crater rim, (2) the area along the steep banksleading into the crater, (3) the basal plain in the crater,(4) an ecotone between woodland and grassland in thecrater and, (5) the central pan. We selected these areasbecause they were consistent with obvious topographicor vegetation changes and we wished to examinewhether these changes coincided with changes in thestable isotope composition of the plants and soils inthe crater. Nine survey stations were set up along aW–E transect (Fig. 1) through the center of the craterin each of the five zones. At each survey station, three6·6-m plots were set up perpendicular to the transect10 m apart. Plants were identified and the plant dis-tributions (% cover) were estimated visually as apercentage of the total plant cover within each plantplot. The plants sampled in the crater were Acacia

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ampliceps Maslin (the salt-water wattle), Aristida latifoliaDomin, Atriplex sp., Crotalaria sp. Cyperaceae, Dol-ichandrone heterophylla (R.Br.) F.Muell., Eragrostissetifolia Nees, Eucalyptus brevifolia F.Muell., Flaveriaaustralasica Hook., Hakea sp., Newcastelia sp.,Melaleuca lasiandra F.Muelland, Ptilotus exaltatusNees, Trichodesma zeylanicum R.Br. and Triodiapungens R. Br. One leaf of each of the species (thenearest to the sampling point) present at each site wascollected. The %C3 and %C4 cover for each wasdetermined by calculating the total percentage ofshrubs, trees and herbs present (C3 vegetation) relativeto the total percent of all grasses, Atriplex sp., Flavariaaustralasica, and sedges present (C4 vegetation). The%C3 and %C4 plant cover for each survey station wasdetermined by averaging the data from the three plots.A soil sample from one of each of these sets of threequadrats was collected for stable isotope analyses ofthe SOM.

Field collection and preparation of samplesfrom the WCMC

Fully expanded, canopy leaves were removed fromplants at 50 stations located along the transect withinWCMC. The location of each station was recorded usinga Global Positioning System (GPS, Garmin 12 XL) andthe data are reported relative to a GPS datum pointtowards the center of the crater (longitude 19�10.310¢Eand latitude 127�47.783¢S). These sites were independentof the sites surveyed using quadrats (described above). Atopographic profile across the crater was carried outusing a Leica TC 1010 (Certified) total station. Theleaves collected were dried in a plant press in the fieldand were then freeze-dried in the laboratory. Approxi-mately 6 cc of the soil surface (0–2 cm, excluding litter)were collected from each of the 50 sites. These weresealed airtight in screw-top Eppendorf tubes. The soilsamples were transported to the laboratory, where the

Fig. 1 a A schematic top viewof the crater; b the change invegetation structure across thecrater

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percentage soil moisture was recorded by subtracting thedry weight (freeze-dried) of the samples of the surfacesoil from the wet weight. A sub-sample of each soilsample was taken and prepared for stable isotope anal-yses by reaction with concentrated HCl in an airtightcontainer to remove any carbonates (Harris et al. 2001)

A sub-sample of the soil samples was used forsalinity and nitrate analyses. Each sub-sample waspacked into a 15-ml conical tube to the 3 ml level. Atotal of 10 ml of distilled water was added to the 13 mlmark and the sample was sealed and shaken vigorously.Each sample was then allowed to settle for 30 min. Theliquid from the conical tubes was removed using apipette and transferred to clean 15 ml conical tubes,which were then sealed and transported to the labora-tory. The sediment was discarded and the retained li-quid was filtered through a pre-combusted glass fiberfilter. The filtrate was tested for salinity using arefractometer (Vista A366ATC). The nitrate concen-tration of the extracts was measured using a LaMottecolorimetric test kit. Measurements of the nitratestandards and samples were conducted on a SchimadzuUV160U UV-visible recording spectrophotometer.Analyses of nitrate solutions of standard concentrationwere used to produce a calibration curve with an r2 of0.99. A water sample was also taken from two of thepools within the central area of the crater (Fig. 1) andtested for salinity. Samples of an algal mat covering thesurface of the pools in the WCMC were taken andfreeze-dried for stable isotope analyses. The positionsof dead Acacia sp. and Eucalyptus sp. trees within thecrater were recorded using the GPS. These were re-corded so as to mark the recent past extent and dis-tribution of these two C3 tree species.

Carbon and nitrogen stable isotope analyses

An aliquot (�0.700 to �0.800 mg of plants and �12.0–16.0 mg of soil samples) of each freeze-dried sample col-lected from the WCMC was weighed into a tin capsule,which was crimped and introduced [via the EA carousel;(Wooller et al. 2001)] into the autosampler (A2100) of aCE Instruments, NA 2500 series, elemental analyzer (EA)at the Geophysical Laboratory (GL). Purified combus-tion gases (CO2 and N2) were separated in a gas chro-matographic column prior to entering a Finnigan ConfloII interface and the stable isotope ratiomass spectrometry(Finnigan MAT, Deltaplus XL). The results are presentedin standard delta notation. Acetanalide (C8H9NO) wasanalyzed (every tenth sample) as a check on the analyticalprecision (and accuracy) throughout the analyses, whichwas±0.2& for d15N (N%=±0.5) and was±0.27& ford13C (C%= ±5.4) (n=26).

Mixing model and statistical analyses

A two-end member mixing model, typical of the typeused in paleoecological studies, to calculate the

proportion of C3 and C4 plants composing past vege-tation, was used to predict the d13C of SOM as follows:

d13CSOM ¼ ð1� X Þd13C‰C3 þ X ðd13C‰C4Þ

where d13C C3=�26.5& and d13C C4=�11.5&, for theaverage values of C3 and C4 plants from the crater,respectively, X=fraction of SOM derived from C4

plants, and (1�X) = fraction of SOM derived from C3

plants. These predicted values were subsequently com-pared with the measured d13CSOM. Use of this modelrelies on the assumption that the modern biomass isincorporated directly into the soil sediment withoutundergoing isotopic fractionation. Where necessary aStudent’s t test was used to determine differences in thestable isotope composition of components (e.g., plantsand soils) from different areas of the crater (e.g., pancompared with basal plain). Error bars for measuredd13CSOM are derived from the d13C of soil for each veg-etation area (Fig. 5a). Error bars for predicted d13CSOM

values are derived from the measurement of %C3 and%C4 of the vegetation in three quadrats placed in eachvegetation area (Fig. 1a).

Results

Vegetation distribution and stable isotope compositionof plants

The Cyperaceae and herbaceous plants Atriplex sp. andFlaveria australasica were classified as C4 (Table 1). Allof the tree species measured from the crater, Acaciaampliceps, Crotalaria sp., Dolichandrone heterophylla,Eucalyptus brevifolia, Hakea sp., Melaleuca lasiandra,Trichodesma zeylanicum, were classified as C3, as werethe herbs Newcastelia sp. and Ptilotus exaltatus. Theleast negative d13Cplant values (��9.6&) were deter-mined in the Cyperaceae samples (Table 1 and Fig. 4)found in the central region of the crater (Fig. 2). TheCyperaceae also had the most variable C/N values,which may have been due to the sedge samples beingsenescent at the time of collection. The algal mat col-lected from one of the pools had relatively less negatived13C values, �14.6&. The grasses Aristida latifolia,Eragrostis setifolia, and Triodia pungens from theWCMC were all classified as C4 according to the d13Cvalues of their leaves (Table 1).

The vegetation in the central (wooded) area of thecrater was dominated by the C3 tree Acacia ampliceps,which varied in height from �7 m at the grassland/woodland ecotone to �2 m at the crater’s center(Fig. 2a). A number of dead Acacia sp. and Eucalyptussp. trees, ranging from 10 cm to 40 cm in diameter atbreast height (dbh), were standing within the woodedarea of the crater. The spatial distribution of the deadEucalyptus sp. trunks seemed to form a circular patternwithin the crater; whereas, the dead Acacia sp. treesseemed to be concentrated around the pools in the crater(Fig. 1).

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The highest d13C value for C3 plants was �23&(Acacia ampliceps), which was measured in the centralpart of the crater (Fig. 3). C3 plants in the region where

Acacia ampliceps is shorter (<4-m high) had a meand13C value of �25.3& ±1.0 (n=24). Conversely, the C3

plants in the outer zone of the crater had some of the

Table 1 Biogeochemical measurements of C3 and C4 plants from the WCMC

Species (sample size) d15N d15N1 SD

d13C d13C1 SD

%C %C1 SD

%N %N1 SD

C/N C/N1 SD

C3–C4*

Acacia ampliceps (n=38) 4.27 3.99 �25.86 1.11 33.6 4.1 2.2 0.5 18.4 4.2 C3

Aristida latifolia �0.9 �11.62 20.8 1.0 24.7 C4

Atriplex sp. (n=7) 16.25 4.23 �11.03 0.95 31.7 3.4 2.5 1.1 22.8 2.1 C4

Crotalaria sp. (n=3) 0.33 1.14 �26.03 1.25 42.0 1.1 2.7 0.4 18.4 2.1 C3

Cyperaceae (n=3) 9.79 3.67 �9.60 0.74 31.7 2.7 1.5 1.2 44.4 40.8 C4

Dolichandrone heterophylla (n=12) 1.55 1.81 �26.19 1.01 38.8 5.9 1.1 0.3 44.7 10.7 C3

Eragrostis setifolia 8.23 �12.08 37.8 1.5 28.7 C4

Eucalyptus brevifolia (n=6) 0.46 0.85 �26.83 1.55 45.1 3.9 1.7 0.7 35.0 15.6 C3

Flaveria australasica (n=9) 6.83 3.59 �12.98 0.71 26.6 3.0 1.6 0.2 20.5 4.0 C4

Hakea sp. (n=4) 4.89 1.13 �27.10 1.36 36.5 9.6 0.6 0.1 70.0 20.1 C3

Newcastelia sp. (n=4) �0.05 1.01 �26.57 1.53 28.4 1.4 0.8 0.1 40.0 5.5 C3

Melaleuca lasiandra (n=15) 0.69 1.89 �27.64 1.07 44.2 7.7 0.9 0.3 61.2 19.6 C3

Ptilotus exaltatus (n=5) 6.68 3.38 �26.09 2.41 29.5 11.7 1.6 0.3 23.1 11.2 C3

Trichodesma zeylanicum (n=7) 1.05 1.19 �26.13 1.04 35.4 1.1 1.8 0.4 24.0 4.4 C3

Triodia pungens (n=21) 1.28 1.50 �11.80 0.68 38.3 7.7 0.8 0.4 66.0 27.1 C4

Algae 6.50 �14.59 7.03 0.4 17.9

*C3 plants (most herbs and woody shrubs) are characterized by d13C values averaging �27& (�21 to �35&) and C4 plants average �12&(�10 to �14&) (Ehleringer 1991)

Fig. 2 a Canopy height ofAcacia ampliceps within theWCMC; b the C3and C4 speciesdistribution across the floor ofthe crater

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lowest d13C values (as low as �30&). The mean d13Cvalue of C3 plants in the region where Acacia amplicepswas absent was �26.5& ±1.5 (n=81). There was nosignificant difference, however, between the d13C valuesof the Acacia ampliceps in the pan compared with thosein the ecotone (t stat=1.2, P‡0.1). With the exception ofFlavaria australasica, the d13C values of the C4 plants inthe central pan were no different from those C4 plantsfrom the rest of the crater (Fig. 4) (t stat=0.2, P‡0.1).The d13C of the halophytic plant Flavaria australasica,which was found in the central pan (Fig. 2) were sta-tistically more negative (by �2&) than the rest of the C4

plants measured from the crater (t stat=2.0, P‡0.001).The d15Nplants values were much higher (up to �20&)

in both the C3 and C4 species inhabiting the central partof the crater compared with those plants in the outerarea (�0&) (Fig. 4). The transition point at which thed15Nplant values increased was abrupt and correspondedwith the ecotone between the grassland and woodland(Fig. 2b). For example, d15Nplant greater than 8& weremeasured in Acacia ampliceps, Ptilotus exaltatus (C3

herb), Eragrostis setifolia (C4 grass) and Flavaria aus-tralasica (C4 herb) (Table 1). The woody species Crota-laria sp., Dolichandrone heterophylla, Eucalyptusbrevifolia, Newcastelia sp. and Trichodesma zeylanicum,which were all present in the outer part of the crater,

all had consistently low (�0–1&) d15Nplant values(Table 1).

The vegetation cover, as determined from the quadratanalysis, demonstrated that there are major differencesin the %C3 and %C4 cover across the WCMC (Table 2).Grasses (Aristida latifolia, Eragrostis setifolia, and Tri-odia pungens) are the dominant plants along the craterbank and the basal plain comprising approximately80–90% of the cover, with some trees (Crotalaria sp.,Melaleuca lasiandra and Hakea sp.) comprising theremaining �20%. Within the pan, trees (primarilyAcacia ampliceps) and herbs comprise �80% of thecover, with a mix of Eragrostis setifolia, Atriplex sp.,Flaveria australasica, and Cyperaceae comprising theremaining �20%.

Soil biogeochemistry

Although the range of d13Csoil values reflected the rangedemonstrated by C3 and C4 plants in the crater (�14 and�22&) the vast majority of these values were interme-diate to d13C of both C3 and C4 plants measured atWCMC. This range of d13Csoil are consistent with thosereported by Bird and Pousai (1997) as a regionaldescription of soils from different biomes in NorthernAustralia. The lowest d13C values from the WCMCoccurred at the ecotone and the most isotopically en-riched values were in the pan (Fig. 5a). Soils from theouter part of the crater and those from the central panhad statistically similar d13C (t stat=0.2, P‡0.1). Thehighest %C values of soils were from the grassland/woodland ecotone compared with soils from the pan orsurrounding plains (Fig. 5b). There was generally goodisotopic agreement between predicted and measuredd13CSOM values for all regions of the WCMC except inthe pan, where predicted values were approximately 8&

Fig. 3 The d13C values of C4 (top panel) and C3 (bottom panel)plants across the floor of the WCMC (hatched area indicates thatthe data is from the Acacia ampliceps woodland/shrubland)

Fig. 4 The d15N values of plants from the WCMC (hatched areaindicates that the data are from the Acacia ampliceps woodland/shrubland)

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depleted relative to measured values (Fig. 6). Our modelused a d13C of �26.5& as the average from the analysesof C3 plants at the WCMC. This value is only �0.5&less negative than the average d13C value from C3 plantsreported by Ehleringer (1991). Of all of the vegetationhabitats, the ecotone showed the largest variation in

terms of the predicted d13C values due to the largevariation in the % composition of C3 and C4 species(Table 2). The ecotone also showed high variability interms of measured d13C values (Fig. 6).

The highest d15Nsoil values were measured from soilsin the central region of the crater (Fig. 5c). Surprisingly,the sharp transition from low to high d15Nplant values atthe ecotone (�0–20&) (Fig. 4) was not evident in thesoil samples measured from the same sites. The lowest(�0&) d15Nsoil values were measured in those samplesfrom the outer area of the crater.

Soil moisture, salinity, and nitrate values were allhigher in the pan relative to the surrounding plains. Thecentral region had the highest concentration of nitrate(�600–10,000 ppm) in the soils (Fig. 7) possibly con-tributing to some of the higher %N values (Fig. 5d). Thedistribution of nitrate in the soils was site specific, andsometimes it was absent from soils at some sites. Therange of nitrate concentrations in the outer region waslower (0–�900 ppm) compared with central region(Fig. 7).

Table 2 The %C3 coverage of 6·6 m quadrats placed in five vegetation habitats in the WCMC

Vegetation sites Mean %C3 (±1 STD) Major C3 plants Major C4 plants

West outer rim 12 (±3) Eucalyptus sp. Triodia pungensEast outer rim 35 (±20) Eucalyptus sp. Triodia pungensWest bank 12 (±8) Eucalyptus sp. Triodia pungensEast bank 14 (±1) Eucalyptus sp. Triodia pungensWest Plain 18 (±26) Eucalyptus brevifolia/Melaleuca lasiandra Triodia pungensEast Plain 15 (±10) Eucalyptus brevifolia Triodia pungensWest Ecotone 55(±34) Acacia ampliceps Eragrostis setifolia/CyperaceaeEast Ecotone 44 (±33) Acacia ampliceps Eragrostis setifolia/CyperaceaeCentral Pan 81 (±13) Acacia ampliceps Flaveria australasica/Cyperaceae

Fig. 6 The predicted (based on the %C3 and %C4 of thevegetation) (filled circles) and measured (nonfilled circles) d13C ofsoil organic matter in the WCMC. Error bars for measured valuesare derived from the d13C of soil for each vegetation area (Fig. 5a).Error bars for predicted values are derived from the measurementof %C3 and %C4 of the vegetation in three quadrats placed in eachvegetation area (Fig. 1a)

Fig. 5 The d13CTOC (a), % C (b), d15N (c) and % N (d) of soilsfrom the WCMC (hatched area indicates that the data is from theAcacia ampliceps woodland/shrubland)

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Soil moisture was an important determinant of themean d15Nplant value from each of the sample stations(r2 = 0.72, n=49). Rather than being strictly linear, therelationship seemed to illustrate two different popula-tions: one in the outer area where the plants had lowd15N values (�0&) and the soil was dry, and the secondin the central region where the plants had higher d15Nvalues (up to �20&) and the soil was wetter. There wasno significant relationship, however, between soil salin-ity and d15N value of plants at the sites (r2=0.18,n=49), although those plants existing in situations withlow soil salinity (0 ppt) had consistently low d15N values(<4&). The salinity of the groundwater measured attwo of the pools was 15 and 19 ppt. High soil salinity inthe central pan is likely the result of these soils beingin contact with this ground water. In addition, high

evaporation relative to precipitation from the pan con-centrates salts even further. The high d15Nplant values atthe center of the crater corresponded with highly salinesoils that range up to �320 parts per thousand (ppt)(Fig. 7b).

Discussion

Modern vegetation distribution and habitat character-istic within the WCMC

Vegetation distribution within the WCMC is likelycontrolled by edaphic conditions. The quadrat analyses(Table 2) and vegetation stable isotope survey (Fig. 2b)verified what is observed from the rim of the crater; C4

grasses dominate the basal plains, C3 trees dominate thecentral pan, and the ecotone is comprised of a mix of C3

and C4 vegetation. The higher moisture content of thesoil in the central part of the WCMC (Fig. 7a) did notseem to confer more favorable growing conditions forthe plants in the crater (based on the height of Acaciaampliceps and total plant cover) most likely because ofhigh soil salinity (Fig. 7b). Salts, including gypsumcrusts, were concentrated in the soil resulting fromevaporative pumping, exacerbating the saline conditionsfor the plants within the central area. A group of halo-phytic plants, including Acacia ampliceps, Atriplex sp.,Eragrostis setifolia, and Flavaria australasica were pres-ent in the central pan. Eragrostis setifolia, for instance, isoften found in swamps and drainage floors that arefrequently saline (Mitchell and Wilcox 1994) and wherethe organic content of the soil is relatively high (Pelhe-ram and Kok 1991; Rye et al. 1992; Watson and Dall-witz 1994). Atriplex species are also often found in salineconditions (Bajji et al. 1998; Cantero et al. 1998; deLange et al. 2000; Khan et al. 2000; Mitchell and Wilcox1994), as are some Hakea species (e.g., Hakea preissiiMeissner) (Mitchell and Wilcox 1994).

Increases in d13C values occur in certain plantsgrowing in saline conditions due to isotopic fraction-ation associated with a need for increased water useefficiency (WUE) (Farquhar et al. 1982; Lin andSternberg 1992). Accordingly, the d13C values of thesmaller trees (Acacia ampliceps) growing on the highlysaline soils of the central pan were up to 8& higherthan for the C3 trees growing outside of the pan(Fig. 3). Sandy, shallow, dry, nutrient-depleted soils ofthe basal plain and crater bank favored establishmentof C4 grasses because they are superior in WUE andnutrient use efficiency (NUE) compared to woodlandspecies (Rye et al. 1992). The halophytic, C4 plantFlavaria australasica was observed as having morenegative d13C values compared to the other C4 plants inthe crater (Fig. 4).

The salinity gradient across the crater was correlatedto a d15Nplant gradient across the crater (Fig. 4). Thed15N of plants towards the center of the crater areunusually high for plants (Handley and Raven 1992;

Fig. 7 The relative soil moisture (a), salinity (ppt) (b), and nitrateconcentration (lmoles/soil extract) (c) of soils from the WCMC(hatched area indicates that the data is from the Acacia amplicepswoodland/shrubland)

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Evans 2001) and yet there are a number of situationsand processes that can yield very positive d15N values.Some high d15N values in plants are the result of anecosystem receiving quantities of guano from marineanimals (Erskine et al. 1998; Wooller et al. 2003b), whichhas a very positive d15N value. This explanation for thehigh d15N values in the plants from the center of thecrater is unlikely given the distance of the site from anymarine environment. Large ranges in nitrogen isotopefractionation can also occur as a result of NO3

� pro-duction during nitrification (15–35&) and NO3

� assimi-lation into organic N by plants (0–19&) (Robinson2001). Although we cannot currently test any of thesehypotheses, given logistical challenges associated withrevisiting the site, there is evidence for relatively highconcentrations of nitrate in patches of the soil in thecentral part of the crater (Fig. 4), which may have be-come enriched in 15N over time. Substrate pools ofnitrogen can become markedly enriched in 15N in closedsystems where there is a limited quantity of substrate.Removal of N from a closed system (which can takemany forms, including plant uptake of N, herbivory,denitrification, and ammonia volatilization) generallyresults in the enrichment of the remaining substrate in15N (Evans 2001; Robinson 2001). The WCMC, whichwas formed �300 ka BP (Shoemaker et al. 1990), mayrepresent a unique, long-term and closed-N system. Thepool of nitrogen available to the plants in the centralpart of the crater could be highly enriched in 15N.Enrichment can result from a number of processes(Robinson 2001) including denitrification, where nitro-gen depleted in 15N is converted to N2, which then leavesthe ecosystem (Kendall 1988). A marked difference be-tween the d15N of the soils and plants in the center of thecrater is apparent. It is possible that the soil d15N valuesare not portraying the d15N values of the N pool that theplants are taking up. The soil d15N values are liable to bea mixture of the organic and inorganic nitrogen pools inthe soil; whereas, the plants are liable to be taking updissolved inorganic nitrogen (DIN) in the ground water(e.g., ammonium). Unfortunately, we did not have asufficient sample of the ground water to measure thed15N of the DIN pools, although it is apparent thatsome areas of the moist, saline, soil in the central part ofthe crater had relatively high concentrations of nitratepresent. Given the sample size (weight of dried plantmaterial) used for d15N analysis, the analytical precisionwe report and the %N of our samples we are confidentthat the high d15Nplant and large degree of variability inthe d15Nplant from toward the center of the crater are nota reflection of analytical variability. Table 1 shows that,generally speaking, the high standard deviations ford15Nplant are associated with the plants with high d15Nvalues. Since these plants are generally the plants withthe higher %N values (Table 1) this would tend tocounter any argument that these values may be the resultof smaller N sample sizes. It therefore seems more likelythat the plants in the central part of the crater arecharacterized by higher and more variable d15N values,

compared with plants from the outer part of the crater.It is possible that the high standard deviation of theseplants is a reflection of a heterogeneous (isotopic andspatial) source of nitrogen. This would seem to be con-sistent with the heterogeneous soil N data, includingd15N data from the analyses of the soil (Fig. 5) and thenitrate concentrations in the soil (Fig. 7). Large intra-plant variation can also result when NO3

� is the primarynitrogen source (Evans 2001). The woody speciesCrotalaria sp., Dolichandrone heterophylla, Eucalyptusbrevifolia, Newcastelia sp. and Trichodesma zeylanicum,which were all present in the outer part of the crater, allhad consistently low d15Nplant values (�0–1&) indicat-ing that they may have been obtaining their nitrogenfrom atmospheric nitrogen fixation by microbes(Kendall 1988). Crotalaria species are known to haveroot nodules, which contain nitrogen fixing bacteria(Giraud et al. 2001).

The high concentrations of nitrate present, mostnotably in the central (wooded) area, seem to haveaffected the vegetation distribution (Fig. 7c). Ptilotusexaltatus, which was found in the central pan, in addi-tion to being favored under high light intensity (Kadner1998), is promoted in fertilized areas (Brennan et al.2000). Cows grazed within the WCMC up until itbecame a National Park. Cow manure and urine musthave accelerated the nitrogen cycling processes whilethey were present. However, nitrogen may also haveconcentrated over a longer time scale in the crater due tothe closed nature of the crater’s catchment. Stablenitrogen isotope values in the plants seem to be the moststriking marker of the salinity and soil chemistry influ-ence on the modern vegetation (Fig. 4).

Paleoecological implications

Paleoecological records based on stable isotopic analysesas well as records of SOM are relatively sparse fromAustralia’s arid zone, with the exception of central andNW Australia (Johnson et al. 1999; Pack et al. 2003). Ofparticular interest in Australia are those areas withsedimentary sequences covering the last 100 thousandyears (ka) before present (BP), because this encompassesthe time when humans arrived in Australia (�50–56 ka)(Bowler et al. 2003; Roberts et al. 1990; Roberts et al.1994; Turney et al. 2001) and when the megafauna be-came extinct (� 46–50 ka) (Miller et al. 1999; Robertset al. 2001). The WCMC was formed �300 ka BP(Shoemaker et al. 1990) and deep sediments from thecrater are therefore a potentially valuable archive ofinformation on the past environmental conditions of thearea, not least because they could preserve stable iso-topic signatures with which to investigate the pastcomposition of C3 and C4 plants at the site. Documentedtemporal shifts between C3 and C4 vegetation over thelast 300 ka would elucidate much information on theenvironmental and climatic backdrop during significantperiods of Australia’s prehistory.

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At the WCMC d15N analyses of organic materialpreserved in a core could provide a valuable marker ofpast halophytic ecosystems. Unfortunately, sufficientnitrogen for d15N analysis from ancient ecosystems isusually only preserved in exceptional sedimentary situ-ations and yet can be very illustrative of past environ-mental conditions (e.g., Schweizer et al. 2005). Thus, thed13C composition of OM is more typically used toreconstruct past environmental conditions based on thepresence or absence of C3 and C4 plants. Researchersoften do not know the d13C of the vegetation that wasfixing carbon under different environmental and climaticconditions. An understanding of the relationship be-tween the modern vegetation and the d13C values ofmodern SOM is a prerequisite for interpreting the d13Cvalues of SOM. The typical two-end-member mixingmodel that we used to predict SOM d13C values isoversimplified. For instance, we determined a discrep-ancy between predicted and measured SOM d13C valuesespecially in the pan (Fig. 6), which could be the resultof a number of factors. First, there was considerablevariation in d13C for C3 plants in the current vegetation.The relatively large variation in the composition of C3

and C4 plants in the crater and the large variability ind13C values from the plants at the site would make theinterpretation of d13C values from a sediment corechallenging.

Second, isotopic fractionation during decay of OMresults in SOM having a slightly different isotopiccomposition from living vegetation. SOM is also typi-cally enriched in 13C relative to the overlying biomassdue to microbial release of isotopically depleted CO2

during respiration (Macko et al. 1993; Meyers and Ish-iwatari 1993 and references therein). Although Bird andPousai (1997) reported little isotopic fractionationaccompanying degradation of organic material fromsoils in Northern Australia, they also showed thatC3-derived carbon is preferentially incorporated into thecoarse size fractions of soils, while C4 derived carbon ispreferentially added to the fine size fractions. Since ourstudy was restricted to the analysis of TOC, it is unlikelythat this difference in size fractions is represented in ourdataset.

Third, our mass balance calculations used only twopools of organic carbon, and did not allow for theincorporation of CAM plants and algal-derived carboninto the SOM. While CAM plants were not evident inthe modern crater incorporation of aquatic algal bio-mass (d13C=�14.59&) may have contributed to thestable isotopic difference between the predicted andmeasured isotopic composition of SOM in the pan.

Last, the ages of the pools of carbon within totalSOM can span a range from modern labile carbon torefractory carbon. Moreover, the surface SOM repre-sents a time-averaged signal of biomass varying from afew years to a few centuries, depending on OM turn-over rates (Krull et al. 2003). An integrated period of afew centuries could feasibly encompass vegetationchanges associated with the normal drought cycles.

Therefore, it is conceivable that the surface soil in thepan actually represents a plant community that is cur-rently not present. If this were the case, the OM derivedfrom the Eucalyptus and Acacia that recently lived in thepan, for example, should be preserved as isotopicallydepleted SOM. There is some evidence of vegetationchanges in the recent past at the WCMC manifest aschanges in the abundance of C3 and C4 biomass in thecrater. For example, the survey of dead trees at the site(Fig. 1) illustrate that many large Acacia sp. and Euca-lyptus sp. trees died within the central wooded area. Thecircular distribution pattern of some of these dead treesimplies a relationship to past fluctuations in ground-water, which could physiologically stress trees in severalways. A significant rise in the water table would floodthe vegetation and restrict root respiration. A less severerise in the water table could bring saline groundwater into contact with the root zone of plants less tolerant ofextreme salinity (e.g., Eucalyptus spp.) (AustralianDepartment of Agriculture 2003). The presence ofMelaleuca lasiandra and Trichodesma zeylanicum, whichare favored in areas that experience intermittent flood-ing, were found in the outer grassland of the crater floor(Fig. 2). Their occurrence here suggests that the craterfloor has experienced ephemeral flooding or even highergroundwater levels in the recent past. Melaleuca species,which are often found in very stressful conditions(Naidu et al. 2000; Rye et al. 1992), are probably able tosurvive the dry conditions in the outer area of the craterfloor by utilizing an adventitious root system, allowingadaptations to fluctuations in water table and permittingsurvival during occasional flooding (Lockhart et al.1999).

Precipitation and groundwater recharge are depen-dent on the Australian monsoon and the summer pen-etration of the ITCZ from the north. The level of theregional water table, and consequently the water table inthe crater, will vary in response to the effective strengthof the monsoon, which varies in its strength andsouthward penetration (Allan 1985; Suppiah 1992), butrarely extends to the WCMC. High-rainfall events in thecrater region are instead associated with transientdepressions, often ex-cyclone in origin, which are posi-tively correlated to years when the monsoonal trough isenhanced. There is clear evidence of this variation in themodern system in historic observations of groundwaterconditions in the crater. Photographs from the 1960sand early 1970s indicate much drier conditions with alower water table illustrated by live large Eucalypts sp.and an absence of Acacia ampliceps in the crater center.In July 1979, the large eucalypts were alive and sink-holes and caves occurred in the gypsum deposits of thecrater center with the water table at least 2 m below thesurface (John Magee, ANU, Personal Communication).At the same time, Lake Gregory, a large terminal lakedown basin, was dry indicating the culmination of anumber of poor monsoon seasons. Subsequent wetteryears in the catchment have seen Lake Gregory at itshighest historically known levels in 1994 and 2001. The

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rise of the water table in the crater to levels observed in1999 and 2001 is presumably a groundwater response tothese wetter years and part of natural variation in thesystem.

Given our data from the modern vegetation it ispossible to see how erroneous palaeoecological infer-ences could be when based on a single proxy of thevegetation (e.g., d13CSOM) and little understanding of themodern ecosystem. For instance, it would be tempting toequate C4-like d13CTOC values [i.e., values less negativethan an average value for C3 plants (�27&) and similarto an average value for C4 plants (�12&)] from a theWCMC sediment sample with a dry C4 grassland, whenin fact the modern ecosystem shows the possibility of ahalophytic ecosystem with C4-like d13CTOC values. Fromthe modern survey of the WCMC, it is apparent thatthere are three possible habitat end members contrib-uting C4-like carbon to the system: (1) algal mats (d13C= �14&), (2) C4 grasses (Triodia pungens=�12&), and(3) halophytic higher plants (d13C Flaveria australasi-ca=�13&, Atriplex sp.=�11& and Eragrostis setifo-lia=�12&).

Compound specific d13C analyses could be applied ina survey of OM in the sediments at the site to distinguishthese C4-like end members, specifically the contributionsfrom algae and higher plants (e.g., Ficken et al. 2002;Wooller et al. 2003a, b, c). In addition, the C26 n-alkanolis particularly abundant in grasses (and sedges) (Bullet al. 2000) and could be used to distinguish grasses andsedges from the other C4 higher plants. However, thesebiomarkers could not distinguish the C4, dry grasslandcommunity (e.g., Triodia pungens) from the halophyticgraminoid community (e.g., Eragrostis setifolia). Otherbiomarkers may also be of use in differentiating halo-phytic from nonhalophytic plant communities. Pre-liminary analysis of higher plant leaf wax lipids indicatesgreater proportions of longer carbon chains in n-alka-noic acids extracted from halophytic plants than innonhalophytic plants from the WCMC (Wilkie andJohnson, unpublished data). Phytoliths, which areknown to exist in the sediments from the site (Wallis2000) could also possibly be used to distinguish differentplants.

Our survey at the WCMC demonstrates that stableisotopic heterogeneity can be present within a verylimited catchment area and over a sharp change invegetation composition. Often this level of detail is notconducted in modern surveys of sites being consideredor used for palaeoenvironmental research. Environ-mental variability (e.g., salinity and nitrate concentra-tions) across the limited area of the WCMC significantlyinfluences the modern vegetation composition at a localscale. Vegetation dynamics resulting from biotic andabiotic environmental characteristics within a smallcatchment area need to be, at the very least, documentedand preferably understood if adequate palaeoecologicalreconstructions are to be made from sites such as theWCMC. In most respects, the initial observations madefrom the crater rim of a central area dominated by C3

plants (Acacia ampliceps) and an outer area dominatedby C4 plants (Triodia pungens) were reflected in thequadrat data, but were not simply reflected in thed13CSOM values.

Acknowledgments We are grateful to the Billiluna aboriginal com-munity, who allowed us to conduct our survey in the WCMC in1999 and 2001. We also appreciated the assistance given by CALM,not least for allowing us to camp at the crater and for all thesupport given by their on-site rangers. We thank Gillian Atkin,Monique Belanger, Stephen DeVogel, Paul Hesse, Damian Kelle-her, John Magee, Gifford Miller, Elizabeth Miller, Nigel Spooner,and Lynley Wallis for their company and assistance during field-work. We thank Gifford Miller and John Magee for surveying thetopography of the crater and supplying us with the data from thesurvey. We also acknowledge Dana Swarth for measuring themoisture content of our soil samples. Our experiments comply withthe current laws of the countries in which they were performed.This work was funded by an NSF grant (ATM 0081876 to MLF).We thank Chris Turney and two anonymous reviewers for theirconstructive and comprehensive suggestions for modifications toour paper.

References

Allan RJ (1985) The Australian summer monsoon, teleconnections,and flooding in the Lake Eyre Basin. Royal Geographic Societyof Australasia (South Australian Branch), Adelaide

Archibold OW (1995) Ecology of world vegetation. Chapman andHall, London

Australian Department of Agriculture (2003) Salinity tolerance ofplants for agriculture and revegetation. http://www.agric.wa.gov.au/environment/land/salinity/measurement/Plant_salt_tolerance.html

Bajji M, Kinet JM, Lutts S (1998) Salt stress effects on roots andleaves of Atriplex halimus L. and their corresponding calluscultures. Plant Sci 137:131–142

Bird MI, Pousai P (1997) Variations of delta C-13 in the surfacesoil organic carbon pool. Global Biogeochem Cycles 11(3):313–322

Bowler JM (1981) Australian salt lakes: a palaeohydrological ap-proach. Hydrobiologia 82:431–444

Bowler JM (1986) Spatial variability and hydrologic evolution ofAustralian Lake Basins—analog for pleistocene hydrologicchange and evaporite formation. Palaeogeogr PalaeoclimatolPalaeoecol 54:21–41

Bowler JM, Johnston H, Olley JM, Prescott JR, Roberts RG,Shawcross W, Spooner NA (2003) New ages for human occu-pation and climatic change at Lake Mungo, Australia. Nature421:837–840

Brennan RF, Webb MG, Crowhurst AM (2000) Yield responses ofmulla mulla (Ptilotus exaltatus Nees.) seedlings to additions ofnitrogen, potassium and phosphorus fertiliser. Aust J Exp Agric40:867–871

Bull ID, Nott CJ, van Bergen PF, Poulton PR, Evershed RP (2000)Organic geochemical studies of soils from the rothamstedclassical experiments-VI. The occurrence and source of organicacids in an experimental grassland soil. Soil Biol Biochem32:1367–1376

Cantero JJ, Leon R, Cisneros JM, Cantero A (1998) Habitatstructure and vegetation relationships in central Argentina saltmarsh landscapes. Plant Ecol 137:79–100

Cassidy WA (1954) The wolf creek, Western Australia, meteoritecrater. Meteoritics 1:197–199

Commonwealth Bureau of Meteorology A. (2003). Climate infor-mation, http://www.bom.gov.au/climate/

Deines P (1980) The isotopic composition of reduced organic car-bon. In: Fontes JC (ed) Handbook of environmental isotopegeochemistry. Elsevier, Amsterdam, pp 187–221

110

Ehleringer JR (1991) 13C/12C Fractionation and its utility in ter-restrial plant studies. In: B Fry (ed) Carbon isotope techniques.Academic, New York, pp 187–200

Ehleringer JR, Cerling TE, Helliker BR (1997) C-4 photosynthesis,atmospheric CO2 and climate. Oecologia 112:285–299

Erskine PD, Bergstrom DM, Schmidt S, Stewart GR, Tweedie CE,Shaw JD (1998) Subantarctic Macquarie Island—a modelecosystem for studying animal-derived nitrogen sources using15N natural abundance. Oecologia 117:187–193

Evans RD (2001) Physiological mechanisms infleuncing plantnitrogen isotope composition. Trends Plant Sci 6(3):121–127

Farquhar GD, Ball MC, Caemmerer S von, Roksandic Z (1982)Effect of salinity and humidity on d13C value of halo-phytes—evidence for diffusional isotope fractionation deter-mined by the ratio of intercellular/atmospheric partial pressureof CO2 under different environmental conditions. Oecologia52:121–124

Ficken KJ, Wooller MJ, Swain DL, Street-Perrott FA, Eglinton G(2002) Reconstruction of a subalpine grass-dominated ecosys-tem, Lake Rutundu, Mount Kenya: a novel multi-proxy ap-proach. Palaeogeogr Palaeoclim Palaeoecol 177:137–149

Giraud SA, Samba E, Lajudie R, Gillis Pd, Dreyfus B (2001)Certaines legumineuses du genre Crotalaria sont specifiquementnodulees par une nouvelle espece de Methylobacterium. CanJ Microbiol 47:503–508

Guppy DJM, Matheson RS (1950) Wolf Creek meteorite crater,Western Australia. J Geol 58:30–36

Handley LL, Raven JA (1992). The use of natural abundence ofnitrogen isotopes in plant physiology and ecology. Plant CellEnviron 15:965–985

Harris D, Horwath WR, van Kessel C (2001) Acid fumigation ofsoils to remove carbonates prior to total organic carbon orcarbon-13 isotopic analysis. Soil Sci Soc Am J 65:1853–1856

Johnson BJ, Miller GH, Fogel ML, Magee JW, Gagan MK, Chi-vas AR (1999) 65,000 years of vegetation change in centralAustralia and the Australian summer monsoon. Science284:1150–1152

Jones RI, King L, Dent MM, Maberly SC, Gibson CE (2004)Nitrogen stable isotope ratios in surface sediments, epilithonand macrophytes from upland lakes with differing nutrientstatus. Freshwater Biol 49:382–391

Kadner R (1998) Influence of light intensity on vegetative growthof Ptilotus exaltatus R Br. Gartenbauwissenschaft 63:152–156

Kendall C (1988) Tracing nitrogen sources and cycling in catch-ments. In: McDonnell JJ (ed) Isotope tracers in catchmenthydrology. Elsevier, Amsterdam, pp 519–576

Khan MA, Ungar IA, Showalter AM (2000) Effects of salinity ongrowth, water relations and ion accumulation of the subtropicalperennial halophyte, Atriplex griffithii var. stocksii. Ann Bot85:225–232

Krull ES, Baldock JA, Skjemstad JO (2003) Importance of mech-anisms and processes of the stabilisation of soil organic matterfor modelling carbon turnover. Funct Plant Biol 30(2):207–2222003

de Lange PJ, Norton DA, Crowcroft GM (2000) Taxonomy,ecology, and conservation of Atriplex billardierei and A-hollo-wayi sp, nov (Chenopodiaceae) in Australasia. N Z J Bot38:551–567

LaPaz L (1954) Meteoritic material from the wolf creek, WesternAustralia, Crater. Meteoritics 1:200–203

Lin G, Sternberg LDL (1992) Effect of growth form, salinity,nutrient and sulfide on photosynthesis, carbon isotope dis-crimination and growth of red mangrove (Rhizophora-mangleL). Aust J Plant Physiol 19:509–517

Lockhart C, Austin DF, Aumen NG (1999) Water level effects ongrowth of Melaleuca seedlings from Lake Okeechobee (Florida,USA) littoral zone. Environ Manag 23:507–518

Macko SA, Parker PL (1993) Early diagenesis of organic matter insediments: assessment of mechanisms and preservation by theuse of isotopic molecular approaches. In: Engel MH, MackoSA (eds) Organic geochemistry. Plenum Press, New York,pp 211–224

McCall GJH (1965) Possible meteorite craters—wolf creek,Australia and analogues. Ann N Y Acad Sci 123:970–998

McKee KL, Feller IC, Popp M, Wanek W (2002) Mangroveisotopic (delta N-15 and delta C-13) fractionation across anitrogen vs. phosphorus limitation gradient. Ecology83(4):1065–1075

Meyers PA, Ishiwatari R (1993) The early diagenesis of organicmatter in lacustrine sediments. In: Engel MH, Macko SA (eds)Organic geochemistry. Plenum Press, New York, pp 185–209

Miller GH, Magee JW, Johnson BJ, Fogel ML, Spooner NA,McCulloch MT, Ayliffe LK (1999) Pleistocene extinction ofGenyornis newtoni: human impact on Australian megafauna.Science 283:205–208

Mitchell AA, Wilcox DG (1994) Arid shrubland plants. Universityof Western Australia Press, Perth

Mora G, Pratt LM, Boom A, Hooghiemstra H (2002) Biogeo-chemical characteristics of lacustrine sediments reflecting achanging alpine neotropical ecosystem during the Pleistocene.Quat Res 58(2):189–196

Naidu BP, Paleg LG, Jones GP (2000) Accumulation of prolineanalogues and adaptation of Melaleuca species to diverseenvironments in Australia. Aust J Bot 48:611–620

O’Leary MH (1988) Carbon isotopes in photosynthesis: fraction-ation techniques may reveal new aspects of carbon dynamics inplants. Bioscience 38(5):328–336

Pack SM, Miller GH, Fogel ML, Spooner NA (2003) Carbonisotopic evidence for increased aridity in northwestern Australiathrough the quaternary. Quat Sci Rev 22:629–643

Pelheram RJ, Kok B (1991) Plants of the Kimberley Region ofWestern Australia. University of Western Australia Press,Nedlands

Reeves FC, Chalmers RO (1948) Wolf creek crater. Aust J Sci11:154–156

Roberts RG, Jones R, Smith MA (1990) thermoluminescencedating of a 50,000-year-old human occupation site in northernAustralia. Nature 345:153–156

Roberts RG, Jones R, Spooner NA, Head J, Murray AS, SmithMA (1994) The human colonization of Australia: optical datesof 53,000 and 60,000 years bracket human arrival at deaf addergorge, Northern Territory. Quat Sci Rev 13:575–583

Roberts RG, Flannery TF, Ayliffe LK, Yoshida H, Olley JM,Prideaux GJ, Laslett GM, Baynes A, Smith MA, Jones R,Smith BL (2001) New ages for the last Australian megafauna:continent-wide extinction about 46,000 years ago. Science292:1888–1892

Robinson D (2001) d15N as an intergrator of the nitrogen cycle.Trends Ecol Evol 16(3):153–162

Rye BL, Hoch BL, Wilson AJG, Wheeler JR (1992) Flora of theKimberley Region. Department of Conservation and LandManagement, Como

Schweizer MK, Wooller MJ, Toporski J, Fogel ML, Steele A(2005). Examination of an Oligocene lacustrine ecosystem usingC and N stable isotopes. Paleogeography, Paleoclimatology,Paleoecology. TBA

Shoemaker EM, Shoemaker CS, Nishiizumi K, Kohl CP, ArnoldJR, Klein J, Fink D, Middleton R, Kubik PW, Sharma P(1990). Ages of Australian meteorite craters—a preliminaryreport. Meteoritics 409

Suppiah R (1992) The Australian summer monsoon—a review.Prog Phys Geogr 16:283–318

Tieszen LL (1991) Natural variations in the carbon isotopic valuesof plants: implications for archaeology, ecology and paleo-ecology. J Archaeol Sci 18:227–248

Turney CSM, Bird MI, Fifield LK, Roberts RG, Smith M, DortchCE, Grun R, Lawson E, Ayliffe LK, Miller GH, Dortch J,Cresswell RG (2001) Early human occupation at Devil’s Lair,southwestern Australia 50,000 years ago. Quat Res 55:3–13

Wallis LA (2000) Preliminary examination of phytolithsrecovered from Wolfe Creek Crater, northwest Australia.Department of Archaeology and Natural History ResearchSchool of Pacific and Asian Stusies, The Australian NationalUniversity

111

Watson L, Dallwitz MJ (1994) The Grass Genera of the World.CAB International, Cambridge

Wooller MJ, Collins B, Fogel M (2001) The elemental analyzersample carousel: loading an autosampler made easy. RapidCommun Mass Spectrom 15:1957–1959

Wooller MJ, Smallwood B, Scharler U, Jacobson M, Fogel M(2003a) Towards a multi-proxy approach to mangrove palae-oecology: a taphonomic study of d13C and d15N values inR. mangle leaves. Org Geogem 34:1259–1275

Wooller MJ, Swain DL, Ficken KJ, Agnew ADQ, Street-PerrottFA, Eglinton G (2003b) Late Quaternary vegetation changesaround Lake Rutundu, Mount Kenya, East Africa: evidencefrom grass cuticles, pollen and stable carbon isotopes. J QuatSci 18:3–15

Wooller MJ, Smallwood B, Jacobson M, Fogel M (2003c) Carbonand nitrogen stable isotopic variation in Laguncularia racemosafrom Florida and Belize: Implications for trophic level studies.Hydrobiologia 499:13–23

112