Sebastian Probst

Vishal Ranjan

Quentin Ansel

Reinier Heeres

Bartolo Albanese

Emanuele Albertinale

Denis Vion

Daniel Esteve

Steffen J Glaser

Dominique Sugny

Patrice Bertet
email: patrice.bertet@cea.fr

Shaped pulses for transient compensation in quantum-limited electron spin resonance spectroscopy

Keywords: electron paramagnetic resonance, arbitrary waveform generator, shaped pulses, superconducting resonators, quantum limited amplifier

In high sensitivity inductive electron spin resonance spectroscopy, superconducting microwave resonators with large quality factors are employed. While they enhance the sensitivity, they also distort considerably the shape of the applied rectangular microwave control pulses, which limits the degree of control over the spin ensemble. Here, we employ shaped microwave pulses compensating the signal distortion to drive the spins faster than the resonator bandwidth. This translates into a shorter echo, with enhanced signal-to-noise ratio. The shaped pulses are also useful to minimize the dead-time of our spectrometer, which allows to reduce the wait time between successive drive pulses.

Introduction

Electron spin resonance (ESR) spectroscopy allows to analyze the composition and structure of paramagnetic samples [START_REF] Schweiger | Principles of pulse electron paramag-385 netic resonance[END_REF]. In the inductive detection method, the sample is coupled to a resonant microwave cavity of frequency 5 ω 0 . When the spins are tuned to ω 0 by application of a magnetic field B 0 , they interact with the magnetic component of the intra-cavity microwave field B 1 (t). After being driven by appropriate microwave pulse sequences, their Larmor precession dynamics induces the subsequent 10 emission of weak microwave spin-echo signals, which carry information on the properties of the paramagnetic species present in the sample.

The cavity has several roles in this process. It amplifies the B 1 driving field by a factor proportional to √ Q (Q be-

15
ing the resonator quality factor), which lowers the incident microwave power requirements. It also amplifies the emitted spin-echo signals by the same factor, which conversely enhances detection sensitivity. On the other hand, the cavity bandwidth κ = ω 0 /Q limits both the spin excitation 20 and spin detection bandwidths, which can be a severe issue since typical electron spin linewidths may exceed κ by far.

The cavity also causes transients in the drive fields which limit the degree of control achieved on spin dynamics, and whose characteristic time scale is given by the cavity field 25 amplitude damping time 2/κ. As a result, the cavity quality factor needs to be carefully optimized for the purpose of a given experiment.

A number of these issues can be mitigated by the use of drive pulses with a more complex time-dependence than 30 a simple rectangular pulse (so-called shaped pulses) [START_REF] Takeda | Active compensation of rf-pulse transients[END_REF][START_REF] Tabuchi | Total com-390 pensation of pulse transients inside a resonator[END_REF], as schematically shown in Fig. 1. Thanks to modern arbitrary waveform generators (AWG) [START_REF] Kaufmann | DAC-board based X-band {EPR} spectrometer with arbitrary waveform control[END_REF], microwave pulses with arbitrary time-dependent amplitude and phase can be generated. If the transfer function between the AWG and 35 the intra-cavity field is known, it is possible to compute the drive pulse shape needed to obtain arbitrary intra-cavity field temporal profiles. This strategy in principle eliminates all the drive pulse distortions caused by the cavity; in particular, spins can be driven with a bandwidth much 40 larger than κ using shaped pulses [START_REF] Doll | Fourier-transform electron spin resonance with bandwidth-compensated chirp pulses[END_REF]. Cavity filtering of the signal emitted by the spins, however, remains unavoidable [START_REF] Doll | Fourier-transform electron spin resonance with bandwidth-compensated chirp pulses[END_REF].

The use of shaped pulses [START_REF] Geen | Band-selective radiofrequency pulses[END_REF] has been proposed and demonstrated first in nuclear magnetic resonance spec-45 troscopy [START_REF] Takeda | Active compensation of rf-pulse transients[END_REF][START_REF] Tabuchi | Total com-390 pensation of pulse transients inside a resonator[END_REF][START_REF] Mehring | Phase Transients in Pulsed NMR 410 Spectrometers[END_REF][START_REF] Rhim | Analysis of multiple pulse NMR in solids. II[END_REF][START_REF] Wittmann | Compensating Pulse Imperfections in Solid-State NMR Spectroscopy: A Key to Better Reproducibility and Performance[END_REF]. They have then been applied in ESR spectroscopy [START_REF] Spindler | Perspectives of shaped pulses for EPR spectroscopy[END_REF] for cavity ringdown suppression [START_REF] Borneman | Bandwidth-limited control and ringdown suppression in high-Q resonators[END_REF][START_REF] Kaufmann | DAC-board based X-band {EPR} spectrometer with arbitrary waveform control[END_REF][START_REF] Franck | Active cancellation A means to zero dead-time pulse EPR[END_REF], wide-band Fourier-transform spectroscopy [START_REF] Doll | Fourier-transform electron spin resonance with bandwidth-compensated chirp pulses[END_REF][START_REF] Doll | Wideband frequency-swept excitation in pulsed EPR spectroscopy[END_REF], increased ENDOR sensitivity [START_REF] Tait | ENDOR with band-selective shaped inversion pulses[END_REF], and optimal control [START_REF] Hodges | Universal control of nuclear spins via anisotropic hyperfine interactions[END_REF][START_REF] Zhang | Coherent Control of Two Nuclear Spins Using the Anisotropic Hyperfine Interaction[END_REF][START_REF] Spindler | Shaped optimal control pulses for increased excitation bandwidth in EPR[END_REF][START_REF] Glaser | Training Schrdingers cat: quantum optimal control[END_REF]. They have also been applied for fast 50 superconducting qubit state manipulation [START_REF] Motzoi | Simple Pulses for Elimination of Leakage in Weakly Nonlinear Qubits[END_REF] and readout [START_REF] Jeffrey | Fast Accurate State Measurement with Superconducting Qubits[END_REF]. Recently, a new generation of ESR spectrometers has been demonstrated, relying on superconducting microresonators and amplifiers cooled at millikelvin tempera-tures to reach sensitivity below 100 spin/ √ Hz [START_REF] Bienfait | Reaching the quantum 490 limit of sensitivity in electron spin resonance[END_REF][START_REF] Eichler | Electron Spin Resonance at the Level of $10ˆ4$ Spins Using Low Impedance Superconducting Resonators[END_REF][START_REF] Probst | Inductive-detection electron-spin resonance spectroscopy with 500 65 spins/$\sqrtHz$ sensitivity[END_REF].

Pulse transients are particularly relevant in these experiments since the superconducting resonators can have high quality factors, in the 10 4 -10 5 range. Here we demonstrate cavity transient compensation using shaped-pulses in such a quantum-limited ESR spectrometer. We show that shaped pulses enable cavity ringdown suppression, wide-band spin manipulation, as well as signal-to-noiseratio enhancement.

Theory

We consider here a cavity with a single input/output port. We describe the intra-cavity field in its rotating frame at frequency ω 0 by the two quadratures X(t), Y (t) expressed in dimensionless units, using standard inputoutput theory [START_REF] Gardiner | Input and output in damped quantum systems: Quantum stochastic differential equations and the master equation[END_REF]. The coupling rate to the input port is denoted as κ c , whereas the total damping rate κ = κ c + κ i also includes the internal cavity loss rate κ i . The cavity is coupled to an ensemble of N spins 1/2 with spin operators S (j)

x,y,z . The equations that govern the evolution of spin j are

     Ṡ(j) x = -∆ j S (j) y + g j Y S (j) z Ṡ(j) y = ∆ j S (j) x -g j XS (j) z Ṡ(j) z = g j XS (j) y -g j Y S (j) x , (1)
where g j is the spin-resonator coupling constant [START_REF] Bienfait | Reaching the quantum 490 limit of sensitivity in electron spin resonance[END_REF] (which is proportional to the amplitude of B 1 at the spin location), and ∆ j = ω j -ω 0 is the detuning from the resonator frequency. These are identical to the usual Bloch equations, with the Rabi frequency given by the product of the coupling constant g j and the corresponding field quadrature amplitude [START_REF] Ansel | Optimal control of an inhomogeneous spin ensemble coupled to a cavity[END_REF]. The cavity field is coupled both to the input drive field quadratures β X,Y (t) and to the spins via

Ẋ(t) = √ κ c β X (t) -κ 2 X(t) - N j=1 2g j S (j) y Ẏ (t) = √ κ c β Y (t) -κ 2 Y (t) + N j=1 2g j S (j)
x .

(

) 2
Equations 1 and 2 enable to compute the intra-cavity field and spin dynamics for a given drive field β X,Y (t), provided the distributions of spin Larmor frequency ρ ∆ (∆) and coupling constant ρ g (g) (caused by the spatial inhomogeneity of the B 1 field) are known. Here we are interested in finding the drive fields β X,Y (t) to achieve a given intra-cavity field profile specified by the quadratures X p (t), Y p (t). This problem is drastically simplified if the field generated by the spins (third term on the right of Eqs.2) is negligible compared to the intra-cavity field produced by the drive field. That is the case when the so-called cooperativity parameter C = j g 2 j /(κ ∆) verifies C

1 [START_REF] Ansel | Optimal control of an inhomogeneous spin ensemble coupled to a cavity[END_REF] ( ∆ being the characteristic width of the ρ ∆ (∆) distribution), which is the usual situation in both NMR and ESR. In the following we will assume to be in this situation. A targeted dynamics [X p (t), Y p (t)] is then obtained with the drive fields

β X (t) = [ Ẋp (t) + κ 2 X p (t)]/ √ κ c β Y (t) = [ Ẏp (t) + κ 2 Y p (t)]/ √ κ c , (3)
which is identical to the formula derived in [START_REF] Takeda | Active compensation of rf-pulse transients[END_REF]. Our target 100 pulse shape in this work is the so-called "bump pulse", defined as

X p (t) = X 0 e -1/[1-( t tp /2 ) 2 ] , Y p (t) = 0 , (4)
for |t| < t p /2, and X p (t) = Y p (t) = 0 for |t| ≥ t p /2. X 0 denotes the maximum amplitude and t p the pulse length. This pulse shape goes smoothly to zero at ±t p /2 and does 105 not need to be truncated, contrary to Gaussian pulses for instance [START_REF] Ansel | Optimal control of an inhomogeneous spin ensemble coupled to a cavity[END_REF]. From Eq.3, the time-dependent drive pulse needed to obtain a bump-shaped intra-cavity field is readily obtained.

In the experiment, we detect the field leaking out of 110 the cavity. The latter contains both the reflected drive pulses, as well as the spin free-induction-decay and echo signals. The output field quadratures are given by the input-output relation

X out (t) = √ κ c X(t) -β X (t) Y out (t) = √ κ c Y (t) -β Y (t). (5)
In the following, we resort to numerical simulations to 115 compare our model to the experimental results. For that, we first compute the distributions ρ g (g) and ρ ∆ (∆). We then discretize these distributions into N g × N ∆ bins of spins with identical coupling and frequency. We integrate N g × N ∆ times Eqs. 1 and finally compute the cavity and 120 output fields using Eqs. 2 and 5. All that precedes is the standard treatment of inductivelydetected magnetic resonance, be it nuclear or electronic. One specific aspect of our experiments is that due to the small mode volume, high quality factor of the supercon-125 ducting micro-resonator, and to the low temperature of the experiments, spins relax towards thermal equilibrium dominantly by spontaneous emission of a microwave photon into the cavity [START_REF] Bienfait | 515 Controlling Spin Relaxation with a Cavity[END_REF] -the so-called Purcell effect. The Purcell relaxation rate for spin j is given by

130 Γ 1,j = κ g 2 j ∆ 2 j + κ 2 /4 . (6)
In our experiments, Purcell relaxation plays no role during a spin-echo sequence because it occurs on a much longer timescale, which is why it was not included in Eqs. 1. It however plays a role in the steady-state polarization profile of the spin-ensemble, because of the dependence of

Materials and methods

The spectrometer is built around a superconducting micro-resonator that was described in [START_REF] Probst | Inductive-detection electron-spin resonance spectroscopy with 500 65 spins/$\sqrtHz$ sensitivity[END_REF]. It consists of an Aluminum thin-film patterned as a lumped-element LC circuit with a 100µm-long, 500 nm-wide inductance, on top of a silicon substrate [see Fig. 1(b)]. This inductance defines the active area of the resonator around which B 1 is sizeable and spins are therefore detected; the corresponding mode volume is ∼ 0.2 pL. Finite-element modelling yields the spatial distribution of the B 1 field generated around the inductance, which in turn allows us to compute the coupling constant density function ρ g (g) needed in the simulations. As explained in [START_REF] Probst | Inductive-detection electron-spin resonance spectroscopy with 500 65 spins/$\sqrtHz$ sensitivity[END_REF], the average coupling constant over the detection volume is found to be g/2π ∼ 450 Hz.

The resonator chip is mounted in a sample holder which is cooled down at 12 mK in a dilution refrigerator. The 50 Ω coaxial line used for delivering the control pulses and collecting the signal is connected to the sample holder with a SMA bulkhead to which an antenna is soldered [START_REF] Bienfait | Reaching the quantum 490 limit of sensitivity in electron spin resonance[END_REF]. By tuning the antenna length, one can adjust the capacitive coupling of the resonator to the line and thus its quality factor (Q ∼ 4 × 10 4 in this work). Spectroscopic measurements allow us to extract the resonance frequency ω 0 /2π = 7.274 GHz, the coupling rate κ c = 7.1•10 5 s -1 , the internal energy loss rate κ i = 2.8 • 10 5 s -1 (measured at the single photon limit), and the total energy loss rate κ = 10 6 s -1 . The corresponding field decay time is 2/κ = 2 µs. An overview of both the low-temperature part of the setup and the room-temperature electronics is schematically shown in Fig. 1(c). The input line is heavily attenuated at low temperatures to thermalize the microwave field close to the cryostat base temperature. A circulator routes drive pulses from the input waveguide towards the sample, and the reflected signal (together with the spin signal) towards the output waveguide. It is amplified first at 12 mK by a quantum-limited Josephson Parametric Amplifier (JPA) [START_REF] Zhou | High-gain weakly nonlinear fluxmodulated Josephson parametric amplifier using a SQUID ar-520 ray[END_REF], then at 4K by a High-Electron-Mobility-Transistor (HEMT), and at room-temperature for the final amplification stage. After demodulation by mixing with the local oscillator, the down-converted signal is sampled by a digitizer yielding the field quadratures I(t), Q(t) (in the following only the signal-carrying quadrature is shown). Note that due to the unusually small resonator mode volume, low microwave powers (of order picoWatt) are needed to drive the spins; as a result, we can measure with the exact same setup both the drive pulses after their reflection at the resonator input and the spin signal, which is useful for the shaped pulses characterization. More details on the resonator, JPA, and spectrometer design, can be found in [START_REF] Bienfait | Reaching the quantum 490 limit of sensitivity in electron spin resonance[END_REF][START_REF] Probst | Inductive-detection electron-spin resonance spectroscopy with 500 65 spins/$\sqrtHz$ sensitivity[END_REF]. In [START_REF] Probst | Inductive-detection electron-spin resonance spectroscopy with 500 65 spins/$\sqrtHz$ sensitivity[END_REF] the spin detection sensitivity was estimated to be 65 spin/ √ Hz for the same setup but with a quality factor of 8 • 10 4 . Assuming that the sensitivity scales like κ (since the echo amplitude scales like 1/ √ κ and the repetition time like κ), we estimate it to be in the present case ∼ 150 spin/ √ Hz. A rapid microwave switch makes sure that the sample is protected from the noise at the amplifier except when the pulses are on. The input line is strongly attenuated at low-temperatures in order to thermalize the microwave field to millikelvin temperature. The pulses are routed to the sample via a circulator, and the reflected signal is routed to the output line. It then undergoes amplification at several stages, starting from a JPA at 12 mK, followed by a HEMT at 4K and then at room-temperature. The signal is finally demodulated using an IQ mixer, and its two quadratures digitized.

One issue with superconducting micro-resonators is their low power handling capability. Indeed, in a superconducting strip such as used for the inductance, non-linear effects appear when the current density approaches the critical current density of the film. For Aluminum at low temper-200 atures it is of order 10 11 A/m 2 [START_REF] Romijn | Critical pair-breaking current in superconducting aluminum strips far below ${T} {c}[END_REF], which implies that in our geometry non-linear effects are expected for ∼ 1 mA ac current in the wire. Because of the large spin-resonator constant however, spins can be driven efficiently well below that threshold as will be shown in the following.

In order to generate microwave drive pulses with arbitrarilycontrolled amplitude and phase, we modulate the continuous signal delivered by a microwave synthetizer (the local oscillator LO) using two analog outputs of an AWG (model Tektronix 5014), using an IQ mixer. The AWG sampling rate is 1 Gs/s, and its analog bandwidth is 300 MHz. After calibration of the IQ mixer, LO leakage was -∼ 60 dB. At the mixer output, the pulse goes through a voltagecontrolled attenuator and is then amplified to obtain sufficient driving strength. Right before the low-temperature part of the setup, a fast microwave switch controlled by a digital output of the AWG with 80 dB dynamics transmits microwave signals into the cryostat only during the application of the drive pulses. This protects the spins from the amplifier output noise, which would otherwise reduce their equilibrium polarization [START_REF] Bienfait | Magnetic Resonance with Squeezed 530 Microwaves[END_REF]. Phase cycling is performed using the IQ modulation by the AWG.

To test the spectrometer operation with shaped pulses, we use the electron-spin resonance of bismuth donors in silicon as a model system. Bismuth atoms were implanted into the silicon sample on which the resonator is patterned, at a typical depth of 100 nm. At low temperatures, bismuth atoms can bind an electron; details on the spin Hamiltonian of such bismuth donors can be found in [START_REF] George | Electron Spin Co-535 herence and Electron Nuclear Double Resonance of Bi Donors in Natural Si[END_REF][START_REF] Wolfowicz | Atomic clock transitions in siliconbased spin qubits[END_REF]. A field B 0 = 3.74 mT is applied in order to tune the lowest-frequency transition of the bismuth donors in resonance with ω 0 . As explained in [START_REF] Bienfait | Reaching the quantum 490 limit of sensitivity in electron spin resonance[END_REF][START_REF] Pla | Strain-Induced Spin-Resonance Shifts in Silicon Devices[END_REF][START_REF] Probst | Inductive-detection electron-spin resonance spectroscopy with 500 65 spins/$\sqrtHz$ sensitivity[END_REF] the spin resonance of the donors in our experiment is broadened by strain in the substrate caused by thermal contraction of the thin-film resonator upon cooling, which affects inhomogeneously the hyperfine coupling constant between the bismuth nuclear and electron spins. The resulting spin linewidth was measured to be of order ∼ 20 -30 MHz [START_REF] Probst | Inductive-detection electron-spin resonance spectroscopy with 500 65 spins/$\sqrtHz$ sensitivity[END_REF], considerably larger than the 200 kHz resonator linewidth. This situation is frequently encountered in ESR spectroscopy.

In the simulations we will therefore model the spin density ρ ∆ (∆) as being a constant.

Experimental results

Shaped pulse characterization

In NMR and ESR experiments using shaped pulses, the intra-cavity field is often characterized by inserting a pickup coil in the resonator [START_REF] Tabuchi | Total com-390 pensation of pulse transients inside a resonator[END_REF][START_REF] Wittmann | Compensating Pulse Imperfections in Solid-State NMR Spectroscopy: A Key to Better Reproducibility and Performance[END_REF][START_REF] Spindler | Shaped optimal control pulses for increased excitation bandwidth in EPR[END_REF], or by using the Rabi nutation of the spins [START_REF] Doll | Fourier-transform electron spin resonance with bandwidth-compensated chirp pulses[END_REF]. Here we directly measure the reflected drive pulse, and use it to extract the intracavity field. This is facilitated by the low microwave power (picoWatts at the sample level) of the drive pulses used in our experiments, which is itself a consequence of the large spin-resonator coupling.

As can be seen from Eq. 5, the intra-cavity field can be obtained by subtracting the reflected signal from the incident drive pulse, both measured with the very same setup. To do so, we measure the reflected pulse at ω 0 , whereas the incident pulse is measured by applying it 10 MHz off-resonance from ω 0 , so that it is fully reflected

Ion (mV) Ioff -Ion (mV) I off (mV)
Figure 2: Reflected quadrature signal of a square (green dots) and bump-shaped (blue dots) pulses, measured 10 MHz off-resonance (i) and on-resonance with ω 0 (ii). Subtraction yields the intra-cavity field (iii). Solid lines are from the theory. The small oscillations probably originate from parasitic resonances in the microwave setup.

at its input without deformation. Because of the small 260 frequency difference, the transfer function of the whole setup can be considered identical in both cases, so that the signals can be simply subtracted, yielding the intracavity field X(t), Y (t).

Examples are shown in Fig. 2 (only the quadrature car-265 rying the signal is displayed). For a 1 µs-long squareshaped pulse, the intra-cavity field shows a linear rise during the pulse, followed by an exponential decay with a time constant of ∼ 2/κ as expected. We then generate a "bump" pulse with t p = 1µs (Eq.4), using Eqs.3 to com-270 pute the AWG drives [START_REF] Takeda | Active compensation of rf-pulse transients[END_REF]. The measured intra-cavity field of the bump pulse is in excellent agreement with the expected pulse shape as given by Eq.4, with the maximum amplitude as the only fitting parameter. Transients are efficiently suppressed, by at least an order of magnitude;

275 and the intra-cavity field rise-and decay time is ∼ 250 ns, an order of magnitude shorter than the cavity field decay time 2/κ. This successful transient suppression also confirms that the resonator remains linear upon application of the drive pulses (square as well as bump).

Echoes with shaped pulses

We proceed with the measurement of spin-echoes, using a π/2 X -τ -π Y -τ Hahn-echo sequence with X/-X phase-cycling on the first pulse. To optimize the pulse amplitude, Rabi nutation data was taken by measuring the 285 integrated echo amplitude A e as a function of the refocusing pulse amplitude for a square pulse shape (see Fig. 3). Damping of the oscillations is caused by the spread in Rabi

I (mV) (a) (b)
x 4000 x 10 θ π/2 Figure 3: (a) Hahn-echo sequence with square and bump-shaped pulses. First, a π/2 X -τ -π Y -τ spin-echo was measured (inset). The corresponding control pulses were sampled immediately afterwards, with only a change in amplifier gain at the detection to compensate for the larger signal amplitude. For convenience, the two control pulses were this time generated on the same quadrature, which is shown here in the main panel. Open circles are data (green for square, blue for bump), and solid lines are results from the simulation (black for square, red for bump). (b) Rabi oscillations (blue dots) and simulation (black line) for a square-shaped-pulse Hahn echo sequence with varying refocusing pulse amplitude. frequency ρ g (g) due to B 1 spatial inhomogeneity, and is qualitatively reproduced by the simulations. Figure 3 also shows the reflected signal quadrature of a full echo trace, including the echo, both for 1µs-long square-shaped and bump-shaped pulses. The reflected control pulses again demonstrate transient suppression in the bump-pulse case. The bump-pulse echo is both shorter and higher-amplitude than the square-pulse. These features are well captured by simulations.

We study the shaped pulse echo in more details in Fig. 4. In order to measure the contribution from spins outside of the cavity bandwidth, a low repetition rate is necessary, since those spins relax more slowly than spins at resonance because of the Purcell effect (see Eq.6). Figure 4 shows a time trace of a Hahn echo, measured using bump pulses with t p = 1µs, and a repetition time t r = 1 s. The echo shows a pronounced asymmetric shape, with a sharp rise in less than a microsecond, and a slower decay. The fact that the echo signal rises faster than 2/κ demonstrates that the echo originates from the rephasing of spins lying in a broader frequency range than the cavity bandwidth. After the echo reaches its peak amplitude, it decays in ∼ 2/κ. Indeed, despite the use of shaped pulses to drive the spins over arbitrarily wide bandwidth, their emission remains unavoidably filtered by the cavity [START_REF] Doll | Fourier-transform electron spin resonance with bandwidth-compensated chirp pulses[END_REF]. To visualize more quantitatively the dynamics of the spin-ensemble magnetization, we have numerically deconvoluted the cavity response (see Fig. 4a inset), resulting in a Gaussian-shaped time dependence with a FWHM width of 1.3µs. The Fourier transform of the magnetization is also shown in Fig. 4, and shows a linewidth 4 times greater than κ. Numerical simulations were performed using the 320 computed distributions ρ g and ρ ∆ , based on the equations of Section II, and taking into account the Purcell relaxation. The echo shape and duration are quantitatively reproduced, as well as the spin magnetization dynamics. One motivation for short control pulse duration is their higher robustness to spin detuning. Indeed, the nutation frequency of spin j is given by ω

2 1 + ∆ 2 j , with ω 1 = g j √ X 2 + Y 2 .
Due to the transient decay, square-shaped pulses have an effective minimum duration of order of 2/κ, implying that the maximum value of ω 1 for a π pulse is ∼ κ. Spins on the edges of the resonator bandwidth (those with ∆ i ∼ κ/2) therefore unavoidably undergo a Rabi nutation with an angle and axis that are significantly different from those at resonance with a square-shaped pulse.

Bump-shaped refocusing pulses on the other hand have a shorter duration, leading to higher ω 1 for a π-pulse and thus to better performance for spins with ∆ i ∼ κ/2. To test this prediction, we compare the signal-to-noise ratio of an echo obtained with the same square-shaped π/2-pulse, but with either a bump-or square-shaped refocusing π pulse. The signal and noise are given by A e = I(t)u(t) dt and σ = δI 2 (t)u 2 (t) dt, respectively, where u(t) represents the mode shape of the echo normalized such that [u(t)] 2 dt = 1 [START_REF] Bienfait | Reaching the quantum 490 limit of sensitivity in electron spin resonance[END_REF]. This mode shape is obtained by fitting a skewed Gaussian function to the echo signal

u(t) = 1 N exp - (t -t 0 ) 2 2σ 2 erfc α t -t 0 σ √ 2 , ( 7
)
where N is the normalization, σ the scale and α the shape 325 factor. We find a SNR improvement of 16% in the bump refocusing pulse case compared to square-pulse refocusing, which confirms the better performance of bump-shaped refocusing pulses. Suppression of cavity ringdown enables to minimize the delay between control pulses, which is particularly useful for dynamical decoupling pulse sequences where refocusing pulses are applied shortly one after the other. As a proofof-principle, we run a Carr-Purcell-Meiboom-Gill pulse sequence using bump pulses. Even with a delay of 10 µs, the echoes are still clearly separated as seen in Fig. 5; whereas with square pulses the minimal separation was found to be closer to 50 µs. Because of the short delay and long coherence time of donors in silicon (particularly with silicon isotopically enriched in nuclear-spin-free 28 Si as in our experiment), ∼ 1000 echoes can be measured in this way (see Fig. 5). Such a long echo train may be used in particular for further increasing the single-shot signal-to-noise [START_REF] Mentink-Vigier | Increasing sensitivity of pulse {EPR} experiments using echo train detection schemes[END_REF][START_REF] Probst | Inductive-detection electron-spin resonance spectroscopy with 500 65 spins/$\sqrtHz$ sensitivity[END_REF].

The shorter inter-pulse delay within the CPMG sequence reduces the sensitivity to higher frequency noise contributions, which enables more echoes to be generated and thus further SNR enhancement. Here, assuming a whitenoise background, the CPMG averaging would translate into a SNR improvement as high as a factor 20. Recent experiments however have shown that this figure is overestimated in the presence of low-frequency or correlated noise, which may occur in experiments with SC resonators due to resonator phase noise [START_REF] Gao | Noise properties of superconducting coplanar waveguide microwave resonators[END_REF][START_REF] Probst | Inductive-detection electron-spin resonance spectroscopy with 500 65 spins/$\sqrtHz$ sensitivity[END_REF] or long-term spin fluctuations.

Conclusions

We have demonstrated cavity ringdown suppression and wide-band spin excitation using shaped control pulses in a high-sensitivity, quantum-limited ESR spectrometer at millikelvin temperatures. So far only bump pulses were used, which were shown to robustly suppress cavity tran-360 sients and increase the SNR of Hahn-echoes by 16%. Implementing optimal control techniques for special-purpose pulse sequences [START_REF] Spindler | Shaped optimal control pulses for increased excitation bandwidth in EPR[END_REF][START_REF] Borneman | Bandwidth-limited control and ringdown suppression in high-Q resonators[END_REF][START_REF] Glaser | Training Schrdingers cat: quantum optimal control[END_REF][START_REF] Kallies | Cooperative broadband spin echoes through optimal control[END_REF] would be a natural next step to further improve the level of spin control achieved. Also, the ringdown suppression demonstrated here would 365 enable to measure spins with short coherence times, bringing quantum-limited ESR spectroscopy one step closer to real-world applications.

Figure 1 :

 1 Figure1: (a) Basic concept. A short microwave pulse with a rectangular envelope (left green line) is sent onto an ESR cavity and is subsequently distorted by the cavity's transfer function. The resulting intracavity field (center green line) then drives the spins for much longer than intended resulting in spin-echo signals which are stretched in time (right green line). In contrast, if a tailored shaped pulse is employed (left blue line), the cavity distortion is compensated. A short intracavity field (center blue line) now drives the spins resulting in wide-band spin manipulation and shorter echo duration. (b) Schematics and optical images of the LC resonator used in the experiment. Dark areas represent the Si substrate while light areas are made of Al. Bi spins are implanted everywhere below the Si surface, in a box-like profile at a depth ∼ 100 nm. The resonator active area is a 0.2 pL volume around the 100µm-long, 500 nm-wide inductance. (c) Technical implementation. Shaped drive pulses are generated by modulating the output of a continuous-wave microwave generator (LO) by two analog outputs of an AWG via an IQ mixer. A rapid microwave switch makes sure that the sample is protected from the noise at the amplifier except when the pulses are on. The input line is strongly attenuated at low-temperatures in order to thermalize the microwave field to millikelvin temperature. The pulses are routed to the sample via a circulator, and the reflected signal is routed to the output line. It then undergoes amplification at several stages, starting from a JPA at 12 mK, followed by a HEMT at 4K and then at room-temperature. The signal is finally demodulated using an IQ mixer, and its two quadratures digitized.

  280

Figure 4 :

 4 Figure 4: (a) Quadrature signal of the emitted echo (open circles) and its effective spin component gSy obtained by de-convolution of the cavity response (filled circles). The measurement is acquired with a repetition time of tr = 1 s. (b) Fast Fourier transform of gSy showing the spectral bandwidth of the echo, much larger than the cavity bandwidth κ/2π. Solid lines are numerical simulations.

Figure 5 :

 5 Figure 5: Averaged CPMG sequence with minimal pulse separation using bump pulses. The π pulses are not visible as they are being canceled by phase cycling.

the relaxation rate on the detuning and coupling constant. We take this phenomenon into account by initializing the density matrix of spin j at t = 0 as ρ j = [-1 + e -Γ1,j tr ]S z , t r being the repetition time of the experimental sequence.

Acknowledgements

We acknowledge technical support from P. Sénat, D.


Séverine Lopez

Emile Benizri

Peter D Erskine

Yannick Cazes

Jean Louis Morel

Gavin Lee

Edi Permana

Guillaume Echevarria

Antony Van Der Ent
email: a.vanderent@uq.edu.au

Biogeochemistry of the flora of Weda Bay, Halmahera Island (Indonesia) focusing on nickel hyperaccumulation

Keywords: biogeochemical cycling, hyperaccumulator, trace element, ultramafic, nickel

Indonesia has one of the largest surface expressions of ultramafic rocks on Earth and in parallel hosts one of the most species-rich floras. Despite the extensive knowledge of the botanical diversity and the chemistry of these substrates, until recently the records for nickel hyperaccumulators in the region have been scant. Identification of native local hyperaccumulator species is the critical initial step for phytomining as these species match ambient bioclimatic, geochemical and physiological conditions. Prior to this research just 11 nickel hyperaccumulators were known from Indonesia. This field-based investigation at Weda Bay revealed the existence of 13 nickel and two cobalt hyperaccumulators. Phylogenetic affinity for nickel hyperaccumulation is diverse and spans several orders but was most frequent in the Malpighiales as in other ultramafic regions of Southeast Asia.

In contrast to global patterns, hyperaccumulation was infrequent in the Phyllanthaceae.

INTRODUCTION

Ultramafic bedrock is part of the upper mantle (peridotite) obducted in continental margins [START_REF] Searle | Obduction processes in ancient, modem and future ophiolites[END_REF]. Such outcrops are widespread but relatively rare, covering > 3% of the surface of the earth [START_REF] Guillot | Serpentinites: essential roles in geodynamics, arc volcanism, sustainable development, and the origin of life[END_REF]. Southeast Asia has some of the largest tropical outcrops in the world with Borneo and Sulawesi together totalling over 23 000 km 2 (van der Ent et al., 2013b;[START_REF] Galey | Ultramafic geoecology of South and Southeast Asia[END_REF]. Ultramafic soils have high concentrations of iron (Fe) and magnesium (Mg), are enriched in nickel (Ni), chromium (Cr) and cobalt (Co), and are phosphorus (P) and potassium (K) deficient [START_REF] Proctor | Vegetation and soil and plant chemistry on ultramafic rocks in the tropical Far East[END_REF]. The atypical soil chemistry has caused the occurrence of distinct vegetation types characterized by relatively low stature and high levels of endemicity [START_REF] Brooks | Serpentine and its vegetation: a multidisciplinary approach[END_REF][START_REF] Proctor | Vegetation and soil and plant chemistry on ultramafic rocks in the tropical Far East[END_REF][START_REF] Rajakaruna | Serpentine: a model habitat for botanical research in Sri Lanka[END_REF]. Hyperaccumulators are unusual plants that accumulate trace elements to exceptional concentrations in their living tissues at orders of magnitude greater concentrations than 'normal' plants [START_REF] Baker | Terrestrial higher plants which hyper accumulate metallic elements[END_REF]van der Ent et al., 2013a). Some of these plants can reach up to 7.6% Ni in leaves (Mesjasz-Przybyłowicz et al., 2004) and up to 16.9 dry Wt% the phloem sap (van der Ent and Mulligan, 2015). Hyperaccumulator plants can achieve such extraordinary levels of accumulation due to enhanced uptake and translocation mechanisms from the roots to the shoots [START_REF] Baker | Accumulators and excluders -strategies in the response of plants to heavy metals[END_REF]1987). Trace element hyperaccumulation is defined as foliar concentrations in excess >300 mg kg -1 of Co, >1000 mg kg -1 of Ni, >10 000 mg kg -1 of Mn when growing in natural habitats [START_REF] Baker | Terrestrial higher plants which hyper accumulate metallic elements[END_REF][START_REF] Reeves | Tropical hyperaccumulators of metals and their potential for phytoextraction[END_REF]van der Ent et al., 2013a).

On a global scale, Ni hyperaccumulation is the most prevalent, with approximately 520 species reported to date, of which just ∼50 hypernickelophores (e.g. hyperaccumulator species with >1 Wt% shoot dry weight) are known globally [START_REF] Reeves | Tropical hyperaccumulators of metals and their potential for phytoextraction[END_REF]Reeves et al., 2018a).

Hyperaccumulation is a rare phenomenon occurring in 0.2% of total angiosperms [START_REF] Baker | Accumulators and excluders -strategies in the response of plants to heavy metals[END_REF][START_REF] Baker | Terrestrial higher plants which hyper accumulate metallic elements[END_REF] and up to two percent of the ultramafic flora (van der Ent et al., 2015b).

The greatest number of Ni hyperaccumulators has been reported from Cuba (130) and New Caledonia (65) (Reeves et al., 2018b;[START_REF] Jaffré | The metal hyperaccumulators from New Caledonia can broaden our understanding of nickel accumulation in plants[END_REF], and recently Sabah (Borneo Island) also emerged as a hotspot for Ni hyperaccumulators with the recording of 25 species (van der Ent et al., 2015b;2016b). Nickel hyperaccumulators can be categorised in either obligate or facultative species, the former restricted to ultramafic soils and displaying hyperaccumulation, the latter with populations on non-ultramafic and ultramafic soils but only displaying hyperaccumulation on the ultramafic soils [START_REF] Pollard | Facultative hyperaccumulation of heavy metals and metalloids[END_REF]. The ecology and natural selection of hyperaccumulator plants is an active field of inquiry, focussing on anti-herbivore defences, allelopathy and biotic interactions [START_REF] Martens | The ecological significance of nickel hyperaccumulation: a plant chemical defense[END_REF][START_REF] Boyd | The significance of metal hyperaccumulation for biotic interactions[END_REF][START_REF] Jaffré | The discovery of nickel hyperaccumulation in the New Caledonian tree Pycnandra acuminata: 40 years on[END_REF]. Nickel hyperaccumulator plants have the potential to be used in phytomining, an environmentally sustainable technology to produce Ni [START_REF] Chaney | Plant uptake of inorganic waste constitutes[END_REF][START_REF] Chaney | Improved Understanding of Hyperaccumulation Yields Commercial Phytoextraction and Phytomining Technologies[END_REF]van der Ent et al., 2015a). In a phytomining operation, hyperaccumulator plants are grown on ultramafic soils, followed by harvesting and incineration of the biomass to generate a commercial high-grade Ni bio-ore [START_REF] Chaney | Improved Understanding of Hyperaccumulation Yields Commercial Phytoextraction and Phytomining Technologies[END_REF][START_REF] Barbaroux | A new method for obtaining nickel metal from the hyperaccumulator plant Alyssum murale[END_REF]Van der Ent et al., 2015a).

Nickel hyperaccumulators have been recorded from at least 40 different plant families [START_REF] Reeves | Hyperaccumulation of trace elements by plants[END_REF], but are most prevalent in the order Brassicales (Brassicaceae, genera Odontarrhena [synonym Alyssum], Arabidopsis, Bornmuellera [synonym Leptoplax], Noccaea) in temperate regions and in the Asterales (Berkheya, Pentacalia, Senecio), the Buxales (Buxaceae; Buxus) and the supraordinal COM clade (Celastrales, Oxalidales, Malpighiales, mainly Euphorbiaceae, Phyllanthaceae, Salicaceae and Violaceae families) in tropical regions. In Southeast Asia, Ni hyperaccumulator plants are predominantly from the Malpighiales order, and particularly the Phyllanthaceae family (van der Ent et al., 2015b;[START_REF] Galey | Ultramafic geoecology of South and Southeast Asia[END_REF]. The Malpighiales is one the most diverse groups of flowering plants, comprising about 8% of all eudicots and 6% of all angiosperms [START_REF] Davis | Explosive Radiation of Malpighiales Supports a Mid-Cretaceous Origin of Modern Tropical Rain Forests[END_REF][START_REF] Korotkova | Phylogeny of the eudicot order Malpighiales: analysis of a recalcitrant clade with sequences of the petD group II intron[END_REF], and hyperaccumulators are mainly represented in the Phyllanthaceae in the genera, Actephila, Antidesma, Breynia, Cleistanthus, Glochidion and Phyllanthus (van der Ent et al., 2015b). The latter is cosmopolitan and the most speciose genus with over 800 species globally, with major centres of diversity in New Caledonia (113 species) and Cuba where Ni hyperaccumulators are numerous [START_REF] Reeves | Nickel-accumulating plants from the ancient serpentine soils of Cuba[END_REF][START_REF] Reeves | Nickel hyperaccumulation in the serpentine flora of Cuba[END_REF]. Limited systematic screening across phylogenetic lineages means that at present there is no comprehensive understanding of the phenomenon, although such efforts are currently underway using XRF devices (Gei et al., 2018) followed by detailed investigations of their ecophysiology using advances techniques such as synchrotron-based X-ray Fluorescence Microscopy (van der Ent et al., 2017a,b). Hyperaccumulator discoveries continue to be made in Southeast Asia, such as Antidesma montis-silam from Sabah [START_REF] Nkrumah | The discovery of nickel hyperaccumulation in Antidesma montis-silam: from herbarium identification to field re-discovery[END_REF], and even new species that are hyperaccumulators, are described, such as Actephila alanbakeri (van der Ent et al., 2016b) and Phyllanthus rufuschaneyi [START_REF] Bouman | Phyllanthus rufuschaneyi: a new nickel hyperaccumulator from Sabah (Borneo Island) with potential for tropical agromining[END_REF] acustylum (Phyllanthaceae) [START_REF] Wither | Hyperaccumulation of nickel by some plants of Southeast Asia[END_REF][START_REF] Reeves | Tropical hyperaccumulators of metals and their potential for phytoextraction[END_REF]. More recently, fieldwork in Sulawesi recorded Sarcotheca celebica (Oxalidaceae) and Knema matanensis (Myristicaceae) as Ni hyperaccumulators (Tjoa, pers. comm.;van der Ent et al., 2013b).

Ultramafic rock is serpentinised to varying degrees, and serpentinite is used to describe rocks containing >50% serpentine group minerals in which the original mineralogy has been changed. Ultramafic rock generally itself only contains 0.16-0.4% Ni [START_REF] Butt | Nickel laterite ore deposits: weathered serpentinites[END_REF] but this increases significantly during surface weathering in humid tropical climates [START_REF] Echevarria | Genesis and behaviour of ultramafic soils and consequences for nickel biogeochemistry[END_REF] becomes atarget. Where they occur, ultramafic ecosystems are renowned for high levels of endemism, especially in Southeast Asia [START_REF] Galey | Ultramafic geoecology of South and Southeast Asia[END_REF] Specifically, the objectives of this research were to screen for the possible occurrence of hyperaccumulator plants, to provide information on the foliar chemistry, and to provide an indicative assessment of the potential for phytomining at Weda Bay Nickel.

MATERIALS AND METHODS

Study area and sample collection

During the fieldwork, a total of 21 non-permanent plots (see Figure 1 for locations and Table 1 for site properties) were made in which 817 herbarium vouchers and associated foliar samples, in addition to soil samples (totalling 85 samples), were collected for laboratory analysis. Plants were screened in the field (>1000 specimens) for Ni hyperaccumulation using dimethylglyoxime impregnated test paper, and after positive reaction detailed samples were collected for these hyperaccumulator plants. This included samples of the rhizosphere soil, root, wood, branches and leaves. In total 13 Ni hyperaccumulators species, 2 Co, 1 Mn and 10 Al hyperaccumulators were discovered, and associated plant tissue samples totalling 316 samples with 46 matching rhizosphere soil samples collected. The current work does not discuss the hyperaccumulator species from Weda Bay, and we refer to Lopez et al. (2019a, b) for more information about the individual hyperaccumulator species and the rhizosphere chemistry. Concentrations of Ni and other elements were determined in the field with a handheld X-Ray Fluorescence (XRF) instrument. Fresh plant leaves were put in paper bags to prevent decomposition before transport to the field station. Leaves were dried at 70°C for five days in a dehydrating oven. Soil samples were collected from the centre of 15 sites. After an elimination of the surface organic plant debris, organo-mineral horizons were sampled at a depth between 0-5 cm below litter and mineral horizons were sampled at a depth of 10-25 cm depending on the soil type in order to avoid the organo-mineral horizon. In all cases, except for Leptosols, it corresponded to either the Cambic horizon or the Ferralic horizon. The 30 soil samples were air-dried and then sieved to 2 mm before storage and analyses.

Chemical analyses of plant tissue samples

Foliar samples were crushed and ground, and a 500-mg subsample was digested in 3 mL concentrated nitric acid (65%) and 1 mL hydrogen peroxide (30%) for 2 hours at 95°C. The digest was diluted to 40 mL with ultra-pure water before analysis with ICP-AES (Liberty II, Varian).

Elements included in the analysis were Ni, Co, Cr, Cu, Zn, Mn, Fe, Mg, Ca, Na, K, S and P. The potential for foliar contamination with soil particulates is a major risk for accurate analysis of foliar elemental composition. This risk is highest in samples of ground-herbs, and lesser so for trees, but it cannot be entirely avoided. Concomitantly high foliar concentrations of Fe (>2500 μg g -1 ) and Cr (>50 μg g -1 ) are an indication for soil contamination as these elements are major constituents of ultramafic soils.

Chemical analyses of soil samples

Soil samples (500 mg subsample) were acid-digested using freshly prepared Aqua Regia (6 mL 37% hydrochloric acid and 2 mL 70% nitric acid per sample) for a 2-hour program and diluted with ultra-pure water to 50 mL before ICP-AES analysis of pseudo-total elements for Ni, Co, Cu, Zn, Mn, Fe, Mg, Ca, Na, K, S and P. Soil pH was measured in a 1:5 soil : water mixture. Exchangeable Ni, Co, Cr and Mn were extracted in 0.0166 M [Co(NH3)6 3+ , 3Cl -] at a soil : solution ratio of 1:20

(2.5 g : 50 mL) and 1 hour shaking time according to international ISO standard 23470 (ISO 23470:2007). Extractable Ni, Cr and Mn in soil samples were obtained from a DTPA-TEA solution (0.005 M diethylene triamine pentaacetic acid, 0.01 M calcium chloride, 0.1 M triethanolamine, pH 7.4) according to [START_REF] Lindsay | Development of DTPA soil test for zinc, iron, manganese, and copper[END_REF] and concentrations in solutions were measured with ICP-AES (Liberty II, Varian). Total C and N and organic C were quantified by combustion at 900 °C with a CHNS analyser (vario MICRO cube, Elementar Analysensysteme GmbH). Soil samples were weighed using a four-decimal balance and weights recorded for correction of the precise weights in the mass balance calculations. Samples were agitated for method-specific times using an end-over-end shaker at 60 rpm and subsequently centrifuged (10 minutes at 4000 rpm). All soil samples were analysed with ICP-AES (Liberty II, Varian) for Ni, Co, Cu, Zn, Mn, Fe, Mg, Ca, Na, K, S and P. The ICP-AES instrument was calibrated using a multi-element standard prepared in each extraction solution and internal standards were used to ensure of the reliability of ICP-AES analysis.

Mineralogical analyses of soil samples by X-Ray Diffraction (XRD)

The dry samples from the soils from the 15 sites were ground and sieved to 80 μm for mineralogical analysis by XRD. X-Ray diffraction (XRD) analysis was performed on the selected samples using a D8 Bruker diffractometer with Co Kα 1 radiation (lambda = 1.7902 Å). The diffractometer is equipped with a (θ, 2θ) goniometer and a position sensitive detector (PSD). X-ray diffractograms were collected on powder samples at room atmosphere and temperature, within the 2theta range [3, 65°], with 0.035° step and 2s collecting time.

Statistical analysis

The ranges and means of the foliar and soil concentrations were calculated. Correlation coefficients between the soil and plant chemistry data were also calculated. These analyses were undertaken using the software packages STATISTICA Version 9.0 (StatSoft), Excel for Mac version 2011 (Microsoft) and R software (version 3.3.1).

RESULTS

Field survey and hyperaccumulator plant species

The Weda Bay area consists largely of a 'mosaic' of secondary vegetation with patches of more intact forest, and vegetation, which have experienced recurrent fires, particularly near the coast (Figure 2). The highest plant diversity was encountered at the Casuarina site (secondary lowland forest on serpentinite) and at Jira (secondary lowland forest on a laterite plateau). Prior to this field survey no Ni hyperaccumulator plants were known from Halmahera Island, and just five hyperaccumulators were known from Indonesia (van der Ent et al. 2013b). The fieldwork yielded 13 Ni hyperaccumulator plants from the locations survey (including Bukit Limber, Sake South, Sake, Sake West, Uni-Uni, Casuarina) (Table 1). The hyperaccumulator plants originated from a range of different families, and several records included families Anacardiaceae, Apocynaceae, Aristolochiaceae, Moraceae, Piperaceae and Rosaceae that were not previously known to contain Ni hyperaccumulating taxa. Several Ni hyperaccumulator species are locally common and occur widespread at Weda Bay, namely R. aff. bengalensis, Planchonella roxburghiana, F. trachypison and T. morotaiense. Burnt vegetation in the coastal areas was relatively species poor but hosted all 13 Ni discovered hyperaccumulator species including at Sake South and Casuarina. Rinorea aff. bengalensis (Violaceae) is clearly closely-related to the widespread R. bengalensis (Sri Lanka to Northeast Australia), but has morphological differences warranting typification as a distinct taxon (J. DeMuria pers. comm.). It occurs as an under-storey shrub or small tree (up to 10 m tall and a bole of 20 cm diameter) in dense secondary vegetation and short-statured forest on Cambisols.

Ficus trachypison is the sole Ni hyperaccumulating taxon from the genus Ficus and the family Moraceae known globally. It is exceedingly common as a pioneer in degraded (burnt) scrub in the coastal areas, such as at Sake River, and Location 2A-C on Hypereutric Cambisols. One of the most interesting species, because it is a facultative Ni hyperaccumulator, is Trichospermum morotaiense (Tiliaceae). This medium to large tree (up to 20 m tall and a bole of 40 cm diameter) occurs mainly in riparian habitats on ultramafic soils (where it hyperaccumulates Ni) and on limestone (where it does not hyperaccumulate Ni). The genus Trichospermum has 36 species occurring predominantly in Malesia but distributed from Malaysia to the Solomon Islands and Fiji and Samoa, with most species in New Guinea [START_REF] Kostermans | A synopsis of the Old World species of Trichospermum Blume (Tiliaceae)[END_REF]. Trichospermum kjelbergii from Sulawesi was one of the first Ni hyperaccumulators to be discovered in Indonesia [START_REF] Wither | Hyperaccumulation of nickel by some plants of Southeast Asia[END_REF]. Planchonella roxburghiana (Sapotaceae) is a medium-sized tree (up to 15 m tall and with a bole of 25 cm diameter) that occurs in medium tall lowland forest (<20 m) on Hypereutric Rhodic Cambisols. This species is slow-growing, judging by its hard timber, and closely related to Planchonella oxyhedra recorded as a Ni hyperaccumulator from Central Sulawesi [START_REF] Wither | Hyperaccumulation of nickel by some plants of Southeast Asia[END_REF]. No Ni hyperaccumulators were found at higher elevations (>500 m asl), such as at Bukit Limber 900-1000 m asl, which has lower montane forest. This may be explained by the low extractability of Ni and acidic pH in the Rhodic Plinthic Ferralsols of this site. Similarly, Ni hyperaccumulators were absent from Uni-Uni, which has Geric Plinthic Rhodic Ferralsols, with the exception of Glochidion moluccanum (Phyllanthaceae). The latter is a pioneer shrub (no more than 3 m tall) that is common in the graminoid scrub at Uni-Uni that has been repeatedly burnt. We refer to Lopez et al. (2019a, b) for more detailed information about the individual hyperaccumulator species.

Soil mineralogy and soil types

The diffractograms of the soils, both organo-mineral (0-5 cm layer) and mineral (10-25 cm layer) horizons sampled on 15 sites (30 soil samples) were acquired to indicate the weathering status of each pedon as well as the nature of the bedrock (e.g. degree of serpentinisation of the peridotite).

Diffractograms from organo-mineral horizons were usually less easily interpreted because of the high background noise created by the high organic matter content. Therefore, the mineralogy of mineral horizons was used to describe soils (Table 2) except for the soil on Limestone for which the best diffractogram was from the organo-mineral horizon (lack of clay minerals in the mineral horizon). Primary minerals derived from ultramafic soils were either from non-serpentinised peridotite (i.e. diopside, enstatite, tremolite, fayalite) or from serpentinite (i.e. talc, serpentine, magnetite). Secondary minerals were mainly clays (smectite group clays, probably montmorillonite in all the cases) and iron oxides (i.e. goethite and hematite). None of the soils had pyroxenes or olivines as major mineral constituents, although some soils contained traces of these minerals (Blue Hill, Casuarina Plot 1, 2B and Woi Mioseng). One soil had tremolite as its major mineral constituent (Casuarina Plot 2). Serpentine (mostly chrysotile and in one case clino-chrysotile: Bukit Limber Plot 1) is the dominating mineral phase in the soils Blue Hill (co-dominating with serpentine), Uni-Uni Plot 1 and Woi Mioseng). Secondary smectites dominate the mineralogy of Blue Hill, and Location 2A, 2B and 2C. The mineralogy of the rest of ultramafic soils was dominated by secondary goethite. Quartz can be considered as a secondary mineral in most of the soils where it is present. Calcite was the only primary mineral detected for the Leptosol of Doromesmesan and only some clays and traces of quartz could be detected in the organo-mineral horizon. The mineral horizon was pure calcite on this soil. The variety of mineralogical profiles (most representative profiles) is shown in Figure 5.

The soils, according to their morphology (field observations), chemistry and mineralogy could be classified as the following types (Table 1): Rendzic Leptosol on Limestone; Hypereutric Leptosols (Hypermagnesic) and Hypereutric Leptic Cambisols (Hypermagnesic) on Serpentinite; Ferralic Rhodic Cambisols on poorly serpentinised Peridotite and Geric Plinthic Ferralsols on nonserpentinised peridotites (including dunite). This variety of soils created a wide array of edaphic conditions from low pH soils with no exchangeable cations, to neutral and high pH soils with a CEC saturated with Mg. Also, the soils varied deeply from very shallow Leptosols (Blue Hill and Doromesmesan) to very deep laterites (Bukit Limber Plots 1 & 2 and Uni-Uni Plot 1), thus providing a wide array of physical properties for ecosystem processes (shallow vs. deep rooting).

Soil chemical characteristics in the surveyed area

Thirty soil samples were derived from (serpentinised) ultramafic bedrock and one was a Rendzic Leptosol on Limestone (Doromesmesan). Chemical properties of mineral (10-25 cm layer) and organo-mineral (0-5 cm layer) soil samples from each site are presented in Tables 3 to 8. These mineral (Table 3) and organo-mineral (Table 4) horizons showed amounts of total Fe ranging from 1.5 to 39.8%, total Mg from 0.8 to 13.3%. They were all characterized by low concentrations of Ca, P (less than 0.04%) and K (less than 0.03%) excepted for the site Location 2C with 0.05 and 0.08 for the mineral and organo-mineral horizons, respectively. These values and the high values of Ni, which ranged from 87 to 13,587 mg kg -1 , confirmed the ultramafic origin of these different soil samples.

The DTPA-extractable elements (such as Ca, Mg, and K) of the organo-mineral horizons (Table 6) had the highest values in comparison to mineral horizons (Table 5), except for Fe and Mg. DTPAextractable Ni concentrations reached 772 mg kg -1 in Sake South soil.

The pH ranged from 4.07 to 8.16 in the mineral horizons (Table 7) and from 4.65 to 8.07 in the organo-mineral horizons (Table 8). Some Ferralsols or soils with Ferralic properties were present in the collection (e.g. soils from Bukit Limber plot 2, Sake West, Uni-Uni plot 1) and their pH ranged from 4.07 to 5.31 for mineral horizons and from 4.65 to 6.59 for organo-mineral horizons, in the lower of the total range. Also, these soils had very low Cation Exchange Capacity (CEC), with values ranging from 2.04 to 5.05 and from 4.32 to 8.66 cmol + kg -1 , respectively for mineral and organo-mineral horizons, compared to the whole collection (from 2.04 to 53.7 and from 4.32 to 64.3 cmol + kg -1 , respectively for mineral and organo-mineral horizons). These soils were characterized by low exchangeable Mg values compared to the whole range of soils: their Mg-CEC ranged from 0.07 to 1.2 and from 0.38 to 4.1 cmol + kg -1 , respectively for mineral and organomineral soils. The other soils were (Hyper)Eutric Cambisols (Hyper)Magnesic and were also widely present in the area. Their pH was higher in general (ranging from 6.06 to 8.16 and from 6.01 to 7.41, respectively for mineral and organo-mineral horizons) and so was their CEC (presence of high-charge clays and higher organic matter contents) which ranged from 4.40 to 53.7 and from 7.49 to 64.3 cmol + kg -1 , respectively for mineral and organo-mineral soils. Most of the CEC values for these Cambisols were above 20.0 cmol + kg -1 . The maximum reported values for Mg-CEC were reported also for these soils and reached 50 and 40 cmol + kg -1 , respectively for mineral and organomineral horizons. The Rendzic Leptosol sampled from the site Doro Mesmesan Limestone Plot 1 showed particular values as it was not ultramafic with alkaline pH, high amount of total Ca and P but low Fe and Mg concentration (Table 3 and4), inducing a Ca/Mg ratio of 36-46. The CEC was also greater in comparison with the other soils. The CEC in all soils was mostly influenced by the organic matter content (Tables 7 and8) and the amount of smectite-type clays in the mineral phases (Table 2).

Soil weathering tends to favour Ca retention on the CEC and Mg leaching [START_REF] Echevarria | Genesis and behaviour of ultramafic soils and consequences for nickel biogeochemistry[END_REF] and exchangeable Ca was greater in organo-mineral horizons than in mineral horizons for all soils, whereas it was the exact opposite for Mg. Therefore, most of the Ferralsols were not Magnesic, whereas all Cambisols were Magnesic or Hypermagnesic.

The mean total Ni concentrations were 4.16 mg g -1 (0.3-14.0 mg g -1 ) and 3.77 mg g -1 (0.1-12.0 mg g -1 ), respectively for mineral and organo-mineral soils. Exchangeable Ni (Ni-CEC) was usually quite low compared to Mg or to Ca (being the major exchangeable cations) and ranged, when detected, from 0.01 to 0.29 cmol + kg -1 in mineral horizons and from 0.01 to 0.39 cmol + kg -1 in organo-mineral horizons. There is no clear contrast between the two horizons: in some soils it was higher in the OM-rich horizons (mostly Ferralsols), whereas it was the opposite in some others (mostly Cambisols). In the Ferralic Rhodic Eutric Cambisol (Magnesic) from Sake South, there was an unusually high concentration of Ni-CEC in both horizons (1.2-1.4 cmol + kg -1 ). In this soil, Ni saturated 6.0 to 8.2 % of the total CEC. The DTPA-extractable Ni (NiDTPA) was moderate to high with 4.0 to 704 and 0.1 to 773 μg g -1 , respectively for mineral and organo-mineral soils. Ferralsols had NiDTPA values ranging from 4.0 to 17 μg g -1 (with lower values in mineral soils), whereas Cambisols had higher values ranging from 14 to 773 μg g -1 . Again, as for Ni-CEC, the greatest values that were above 700 μg g -1 also corresponded to the soil from Sake South, which is somewhat an intergrade soil between Cambisols and Ferralsols.

Plant foliar chemistry

The 724 leaves from non-hyperaccumulator plants and the 93 leaves from Ni-hyperaccumulator plants were sampled in 21 different ultramafic sites. Based on concentrations measured in soil and foliar parts, the accumulation potential of different elements (Na, Mg, Al, P, S, K, Ca, Mn, Fe, Ni and Zn) was presented for non-hyperaccumulator (Figure 6A) and Ni-hyperaccumulator (Figure 6B) plants. Based on a nonparametric Wilcoxon-Mann-Whitney statistical test, there were significant differences between the ability of non-hyperaccumulator and hyperaccumulator plants to extract all the elements considered.

For the three elements Ca, K and P, plants can be considered as accumulators, with a concentration in their leaves greater than the concentration in soils. This observation was the same whatever the plants; hyperaccumulators or non-hyperaccumulators. Indeed, the mean foliar concentrations were around 15 g kg -1 for Ca, 7.9 g kg -1 for K and 530 mg kg -1 for P (Supplementary information, Tables 1 and3). These very low foliar P concentrations were typical for tropical rain forests plants, as observed by many authors [START_REF] Vitousek | Nutrient cycling in moist tropical forest[END_REF][START_REF] Kitayama | Soil phosphorus fractionation and phosphorus-use efficiencies of tropical rainforests along altitudinal gradients of Mount Kinabalu, Borneo[END_REF][START_REF] Vitousek | Terrestrial phosphorus limitation: mechanisms, implications, and nitrogen-phosphorus interactions[END_REF]. Conversely, hyperaccumulator and non-hyperaccumulator plants here should be considered as excluders for Mg and Mn; these elements showed lower concentrations in plant parts in comparison with those measured in soils whatever the plant considered (Supplementary information, Table 1 to 4). In total, 10 different Al hyperaccumulator plants were recorded (Table 10). There were 5 other Al hyperaccumulator records exceeding the nominal threshold (>1000 mg kg -1 ), but these plants remain unidentified. The identified Al hyperaccumulators were phylogenetically diverse (originating from 7 different families), although three species of Symplocos (Symplocaceae) were prominent at higher altitudes in cloud forest on Bukit Limber. The highest concentration was found in Symplocos maliliensis with 46 300 mg kg -1 foliar Al. Symplocos is a well-known genus of Al hyperaccumulators from Southeast Asia [START_REF] Chenery | Aluminium in the plant world[END_REF][START_REF] Schmitt | Aluminium Accumulation and Intra-Tree Distribution Patterns in Three Arbor aluminosa (Symplocos) Species from Central Sulawesi[END_REF].

There were clear differences concerning foliar concentrations of the elements Al, Fe, Na, S, Zn and Ni (Supplementary information, Tables 1 to 4), between the two plant types (i.e. Ni hyperaccumulator and non-hyperaccumulator plants). For example, Al leaf concentrations for Ni hyperaccumulator and non-hyperaccumulator plants were around 20 and 210 mg kg -1 , respectively, with a concentration 10.5 times greater for non-hyperaccumulators. This is due to the fact that the higher concentration for Ni hyperaccumulators was around 260 mg kg -1 while it was around 35 000 mg kg -1 for other plants, including Al hyperaccumulators obviously. All Al hyperaccumulators (that did not accumulate Ni at all) were reported from sites with Ferralsols (Uni-Uni plot 2, Bukit Limber plots 1 & 2 and Jira plot 1). Conversely, the foliar concentrations for Na and S were higher for hyperaccumulator plants in comparison with non-hyperaccumulators: the concentrations were around 1700 and 1300 mg kg -1 for Na and 2300 and 1900 mg kg -1 for S, respectively for hyperaccumulator and non-hyperaccumulator plants, revealing a higher capability of the hyperaccumulator plants to extract these elements (Na and S). The same trend was observed for Zn. Indeed, we found a three-fold higher Zn concentration in Ni hyperaccumulators with approximately 70 mg kg -1 , while the concentration in other plants was around 25 mg kg -1 .

The most important difference was found in the foliar concentrations of Ni hyperaccumulators vs. non-hyperaccumulators. The mean Ni concentration was ∼5500 mg kg -1 for the hyperaccumulators, while it was ∼230 mg kg -1 for the non-hyperaccumulators. These important differences between non-hyperaccumulator and hyperaccumulator samples were underlined by the distribution, based on the Ni concentrations in leaves, of the number of non-hyperaccumulator samples and hyperaccumulator samples (Figures 6 and8). Moreover, a clear difference between these two types of plants was highlighted, particularly for most of the measured elements in the leaves (Al, Ca, Fe, K, Na, Co, S and Zn). Indeed, the distribution of leaves samples concerning the different elements, such as Fe, Mn, Na and Zn, confirmed the trend that the Ni hyperaccumulator plants can extract higher amounts of these elements, in comparison with the non-hyperaccumulators. The same trend was observed for Co with concentrations around 35 and 2.5 mg kg -1 , respectively for hyperaccumulator and non-hyperaccumulator plants, revealing a concentration 14 times greater for hyperaccumulators.

As shown in Figure 7, based on the DTPA-extractable metal concentrations measured in soils and Ni concentrations in plant parts, Ni hyperaccumulator plants have a higher ability to extract other strategic metals such as Mn, Co and Zn compared to non-hyperaccumulator plants. The difference is not clear for Mn, with a ratio of DTPA-extractable metal present in the soil and leaf concentration of 6.9 and 5.6 for hyperaccumulators and non-hyperaccumulators, respectively. Zn nonhyperaccumulator plants were able to concentrate in their foliar parts 9.5-times the DTPAextractable Zn present in the soil, whereas the hyperaccumulator plants showed a ratio of 25.5, i.e.

2.7-times more in comparison with non-hyperaccumulator plants. For Co, the nonhyperaccumulator plants showed a foliar concentration equivalent to that of the DTPA-extractable Co concentrations found in the soil, but the hyperaccumulator plants were able to concentrate this metal about 14-times more in comparison with non-hyperaccumulator plants. Based on the comparison of foliar metal concentrations and DTPA metal concentrations present in the soil, the best comportment appeared for Ni. Indeed, the non-hyperaccumulator plants concentrated this element up to 1.5-times, while the concentrations in the areal parts of hyperaccumulator plants were 27.5-times higher than the DTPA concentrations in soils, that to say 19-times more than the nonhyperaccumulator plants.

Parasitic mistletoe on the Ni (hyper)accumulator Ficus trachypison

The mistletoe Amyema cuernosensis (Loranthaceae) was recorded parasitizing on the Ni (hyper)accumulator F. trachypison near the Casuarina site (Figure 9, Table 11). It accumulated up to 341 mg kg -1 Ni which can only be acquired from the host since it is an obligate parasite with no root system. The Ni concentrations in the stem and in the leaves of the host plant, i.e. F. trachypison, were 3.0 and 217 mg kg -1 Ni respectively.

DISCUSSION

The specific genesis and geochemistry of ultramafic soils is crucial to understand the occurrence of hyperaccumulation and Ni hyperaccumulators [START_REF] Echevarria | Genesis and behaviour of ultramafic soils and consequences for nickel biogeochemistry[END_REF]van der Ent et al., 2016a). It was not always possible during this survey to access the bedrock at each location in order to describe it, but when it was and described, it was clear that the soil characteristics (soil genesis and functioning) was highly influenced by the degree of serpentinisation of the peridotite (van der Ent et al., 2018a).

The areas covered by strongly serpentinised peridotite or serpentinite always had Cambisols with neutral pH and Mg as the main exchangeable cation in the CEC. These soils had very high level of available Ni. These Hypereutric Cambisols (Hypermagnesic) are derived from strongly serpentinised ultramafic bedrock in which the most important Ni-bearing phases are likely hydrous and crystalline ferrous oxides and smectite minerals in which Ni is either sorbed or included in the crystal lattice [START_REF] Echevarria | Genesis and behaviour of ultramafic soils and consequences for nickel biogeochemistry[END_REF]. Like other ultramafic soil covers in tropical areas [START_REF] Proctor | Vegetation and soil and plant chemistry on ultramafic rocks in the tropical Far East[END_REF][START_REF] Echevarria | Genesis and behaviour of ultramafic soils and consequences for nickel biogeochemistry[END_REF], the mineralogy of Cambisols on serpentinite at Weda Bay was often dominated by smectites in the weathered horizon (BW). The Ferralsols presented several degrees of evolution, probably because of the hilly landscape that induces soil erosion and rejuvenation [START_REF] Echevarria | Genesis and behaviour of ultramafic soils and consequences for nickel biogeochemistry[END_REF]. The most developed soil profiles were found at high altitude on the plateau at Bukit Limber (ca. 1000 m asl.) and at Uni-Uni at a lower altitude (ca. 260 m asl.). The former had the deepest profile development with a 30-m lateritic development in places (as was visible from a mining test pit). The ultramafic region at Weda Bay has therefore a varied gradient of tropical ultramafic pedogenesis.

One surprising finding was that the highest DTPA-extractable Ni concentration ever recorded in an ultramafic soil [START_REF] Echevarria | Genesis and behaviour of ultramafic soils and consequences for nickel biogeochemistry[END_REF]van der Ent et al., 2018a) In contrast, Geric Ferralsols such as at Uni-Uni plot 2, or Bukit Limber plots 1 and 2 have no occurrence of Ni hyperaccumulators and this may be explained by their physico-chemical characteristics: these soils had low DTPA-extractable Ni concentration, acidic pH, and a mineralogy dominated by goethite and hematite which resulted in a very low CEC. However, the DTPA-extractable Al in these soils was high (up to 45 mg kg -1 ) although ultramafic bedrocks are relatively poor in Al, and these soils host Al hyperaccumulators from families or groups that were previously known to contain Al hyperaccumulator taxa in nearby tropical regions: e.g. three different species of Symplocos (Symplocaceae), one species of Syzygium (Myrtaceae), one species of Melastoma (Melastomataceae), one species of Psychotria (Rubiaceae), and several species from the Lauraceae, Theaceae and Cunoniaceae families. Therefore, Ni and Al hyperaccumulation were found in contrasted edaphic situations which was confirmed by the foliar chemistry data from Weda Bay, but also from nearby Sabah (van der Ent et al., 2018b).

Laboratory analysis with ICP-AES confirmed the indicative results achieved from the initial testing in the field with DMG-test paper. Field-testing with DMG paper therefore remains a reliable and quick method for Ni hyperaccumulator reconnaissance. After analysis, the highest Ni concentrations in hyperaccumulator leaves were found in the shrub R. aff. bengalensis and in the tree P. roxburghiana. Both species were hypernickelophores (with foliar Ni concentrations usually above 1.0 %) and were only reported in soils with high DTPA-extractable Ni. In total four species from the 18 hyperaccumulators reported could be considered as metal crops (high biomass, high Ni accumulation), these were: R. aff. bengalensis, F. trachypison, T. morotaiense and G. moluccanum.

Of these species, F. trachypison, T. morotaiense and G. moluccanum appeared to be facultative Ni hyperaccumulator species and pioneer species suitable for first-phase implementation on minerals waste. Rinorea aff. bengalensis, is a strong Ni hyperaccumulator and could be cropped as an understory shrub under the cover of species such as T. morotaiense in the second stage of agromining and then coppiced for efficient Ni phytoextraction.

From the plants collected at Weda Bay, two specimens of R. aff. bengalensis showed Co hyperaccumulation. Both were collected at the location 'Tanjung Ulie'. High foliar Co concentrations had already been reported in the strong Ni hyperaccumulators Rinorea javanica (Violaceae) with up to 670 μg g -1 in natural conditions [START_REF] Brooks | Cobalt and nickel in Rinorea species[END_REF][START_REF] Lange | Copper and cobalt accumulation in plants: a critical assessment of the current status of knowledge[END_REF]. The strong affinity of Mn-oxides for Co may explain the lower Co mobility in Mn-rich soils [START_REF] Collins | Pedogenic factors and measurements of the plant uptake of cobalt[END_REF]. When soils are waterlogged, Co is associated mainly with amorphous Fe oxides after the reduction of Mn and the dissolution of Mn-oxides, and thus becomes more available [START_REF] Lange | Copper and cobalt accumulation in plants: a critical assessment of the current status of knowledge[END_REF]. These conditions are also responsible for the high Co concentrations observed in some Rinorea species as observed for other species, such as Berkheya coddii in South Africa [START_REF] Lange | Copper and cobalt accumulation in plants: a critical assessment of the current status of knowledge[END_REF].

The occurrence of parasitic mistletoes on hyperaccumulator plants is a very rare phenomenon, and has not previously been reported in tropical species or woody hyperaccumulator plants/mistletoes.

The herbaceous Orobanche nowackiana parasitizes the Ni hyperaccumulator Alyssum murale in

Albania while accumulating up to 299 mg kg -1 in its leaves [START_REF] Bani | Relationship between the Ni hyperaccumulator Alyssum murale and the parasitic plant Orobanche nowackiana from serpentines in Albania[END_REF]. Similarly, [START_REF] Reeves | The hyperaccumulation of nickel by serpentine plants[END_REF] reported O. rechingeri parasitizing Alyssum lesbiacum while accumulating more than 600 mg kg -1 Ni. The only other now example is the American Cuscuta californica parasitizing the herbaceous Ni hyperaccumulator Streptanthus polygaloides reaching up to 800 mg kg -1 Ni [START_REF] Boyd | l. The nickel hyperaccumulator Streptanthus polygaloides (Brassicaceae) is attacked by the parasitic plant Cuscuta californica (Cuscutaceae)[END_REF].

With only a small portion of the ultramafic flora of Indonesia screened for Ni hyperaccumulation, this field survey considerably extends the list of Indonesian Ni hyperaccumulators. It is expected that more Ni hyperaccumulators will be discovered in the near future in this country because it has the largest ultramafic extension worldwide with a highly diverse flora (van der Ent et al., 2013b).

Many hyperaccumulator plants are rare, with restricted ranges on ultramafic soils, making them sensitive to destructive forces of mining and forest fires [START_REF] Whiting | Research priorities for conservation of metallophyte biodiversity and their potential for restoration and site remediation[END_REF][START_REF] Erskine | Sustaining metal-loving plants in mining regions[END_REF], and this adds to the urgency for screening to avoid this valuable biological resource from being lost before its known. Table 2. Mineralogy of the soils (Mineral horizons -10-25 cm layer) sampled at each site. For the soil in Doromesmesan, the mineralogy was based on the organo-mineral Horizon (0-5 cm layer). +++ (most abundant mineral); ++ (abundant mineral); + (frequent mineral); (+) (detectable traces).

Table 3. Total elements for mineral soil (10-25 cm layer) samples from each site. Table 4. Total elements for organo-mineral soil (0-5 cm layer) samples from each site.

Table 5. DTPA-extractable elements for mineral soil (10-25 cm layer) samples from each site. Table 6. DTPA-extractable elements for organo-mineral soil (0-5 cm layer) samples from each site. Table 7. pH, exchangeable cations (cmol + kg -1 ) and nitrogen and carbon content for mineral soil (10-25 cm layer) samples from each site. Abbreviations: Cation Exchange Capacity (CEC), % of soil total nitrogen (%N), % of soil total carbon (%C), % of soil organic carbon (%Corg).

Table 8. pH, exchangeable cations (cmol + kg -1 ) and nitrogen and carbon content for organo-mineral soil (0-5 cm layer) samples from each site. Abbreviations: Cation Exchange Capacity (CEC), % of soil total nitrogen (%N), % of soil total carbon (%C), % of soil organic carbon (%Corg).

Table 9. Ni distribution in leaf samples (mg kg -1 ) and soil samples for each site. Abbreviations: Extractable Ni (Ni-DTPA, mg kg -1 ), Exchangeable Ni (Ni-CEC, cmol+ kg -1 ) and Ni total (Ni-T, g kg -1 ), no data (n.d).

Table 10. Aluminium (mg kg -1 ) hyperaccumulator plant records (identified and unidentified specimens) from the Weda Bay area. 8. pH, exchangeable cations (cmol + kg -1 ) and nitrogen and carbon content for organo-mineral soil (0-5 cm layer) samples from each site.

Abbreviations: Cation Exchange Capacity (CEC), % of soil total nitrogen (%N), % of soil total carbon (%C), % of soil organic carbon (%Corg). 9. Ni distribution in leaf samples (mg kg -1 ) and soil samples for each site. Abbreviations: Extractable Ni (Ni-DTPA, mg kg -1 ), Exchangeable Ni (Ni-CEC, cmol+ kg -1 ) and Ni total (Ni-T, g kg -1 ), no data (n.d).

Sites

  both from Sabah. The search for hyperaccumulators has been limited to date in Indonesia. Analysis of herbarium specimens originating from Indonesia led to the discovery of the following Ni hyperaccumulators: Rinorea bengalensis, R. javanica (Violaceae), Trichospermum kjelbergii (Tiliaceae), Planchonella oxyhedra (Sapotaceae), Myristica laurifolia var. bifurcata (Myristicaceae), Brackenridgea palustris subsp. kjellbergii (Ochnaceae), Psychotria sp. (Rubiaceae), Phyllanthus insulae-japen and Glochidion aff.

  . At the same time, ultramafic outcrops holding Ni-rich laterites are Ni mining targets in the Indonesian region. That brings the minerals industry capitalizing on Ni resources in direct conflict with biodiversity. The Weda Bay project in Halmahera has a contract area of 54 874 ha with an estimated resource of 5.1 Mt of Ni and targeted annual capacity of 65 kt yr -1 in Ni. This study aims to provide baseline data on the biogeochemistry of the ultramafic soils of Weda Bay Nickel (WBN) mine lease on Halmahera Island in Indonesia.

  was from a soil that was not a typical Hypereutric Cambisol (Hypermagnesic). It was a Ferralic Cambisol (Magnesic), halfway between a typical ultramafic Hypermagnesic Cambisol and a Geric Plinthic Rhodic Ferralsol. This soil was very rich in total Ni (1.4 %) and had a pH of 5.92. The soil hosted strong Ni hyperaccumulators (some displaying Ni concentrations in their leaves above 2.2 %) although a study in Sabah (Borneo Island) showed that Ni hyperaccumulators are absent from acidic soils (i.e. soils with pH <6.3) and consistently occur on soils with relatively high DTPA-extractable Ca, Mg and Ni concentrations (van der et al., 2016c). It appears that the very high extractability of Ni in the soils were more important than pH conditions for Ni hyperaccumulators. With the exception of the soil at Sake South, the situation at Weda Bay was similar to that of Sabah, with all Ni hyperaccumulators occurring on eroded hypermagnesic Cambisols with (extremely) high DTPA-extractable Ni concentration. These shallow hypermagnesic Cambisols host a xerophytic adapted vegetation in which Ni hyperaccumulators were common, and this aligns with reports from other tropical ultramafic regions, for example in Cuba, New Caledonia, Sabah and the Philippines (van der Ent et al., 2016a).

FIGURE CAPTIONS Figure 1 .

 CAPTIONS1 FIGURE CAPTIONS

Figure 2 .

 2 Figure 2. Aerial views of the landscapes at Weda Bay, Halmahera, Indonesia. Panel A shows exposed serpentinite bedrock in a rock fall near Jira with forest dominated by Casuarinaceae; panel B showing a riverbed upstream of the site of panel A with serpentinite bedrock and a short scrubby vegetation; Panel C shows mature riverine further downstream; panel D shows burnt vegetation on Plinthic Geric Rhodic Ferralsols near Uni-Uni.

Figure 3 .

 3 Figure 3. Ground-level views of vegetation types at Weda Bay, Halmahera, Indonesia. Panel A shows mature riverine forest at the site "Serpentinite River"; panel B shows mature forest near site Casuarina' panel C shows burnt 'maquis-type' vegetation characterised by sedges (Cyperaceae) on Geric Plinthic Rhodic Ferralsols at Uni-Uni, and panel D shows young forest dominated by Macaranga spp. (Euphorbiaceae) on Ferralic Rhodic Hypereutric Cambisols (Hypermagnesic) at Sake River.

Figure 4 .

 4 Figure 4. Soil profiles at key localities at Weda Bay, Halmahera, Indonesia. Panel A shows Hypereutric Cambic Skeletic Leptosols (Hypermagnesic) at the site "Blue Hill"; panel B shows Geric Plinthic Rhodic Ferralsols; panel C shows ferrocrete with plinthic nodules consisting mainly of hematite; panels D and E show Hypereutric Cambisols (Hypermagnesic) at the sites Casuarina and Sake West; panel F shows Geric Plinthic Rhodic Ferralsols at Uni-Uni.

Figure 5 .

 5 Figure 5. X-Ray Diffractograms of the fine earth fraction (< 50 mm) of the B horizons of 5 representative profiles on ultramafic bedrock and of the A-organo-mineral horizon of the Rendzic Leptosol on Limestone. CALC=Calcite; DIOP=Diopside; ENST=Enstatite; GIBBS=Gibbsite; GOET=Goethite; HEM=Hematite; MAGN=Magnetite; QUARTZ=Quartz; TREM=Tremolite; SERP=Serpentine.

Figure 6 .

 6 Figure 6. Plant part and soil total concentrations of different elements for non-hyperaccumulator plants (A) and hyperaccumulator plants (B). All concentrations are expressed as mg kg -1 dry mass.

Figure 7 .

 7 Figure 7. Correlations between element concentrations in plant parts (natural logarithm scale) and number of hyperaccumulator (93 samples) and non-hyperaccumulator (724 samples) plants.

Figure 8 .

 8 Figure 8. Plant foliar and soil bioavailable concentrations with DTPA extractions of different elements for non-hyperaccumulator plants and hyperaccumulator plants. All concentrations are expressed as mg kg -1 dry mass.

Figure 9 .

 9 Figure 9. The mistletoe Amyema cuernosensis parasitizing the Ni hyperaccumulator Ficus trachypison near the Casuarina site. Panel A shows the while mistletoe plant attached to the host; panel B shows the inflorescences of Amyema cuernosensis; and Panel C shows a section of woody stem of Ficus trachypison with the mistletoe stems attached with haustoria.

(

  Loranthaceae) and the host Ficus trachypison (Moraceae).

Figure 1 .

 1 Figure 1. Map of the field sampling sites and the location of Weda Bay on Halmahera Island, Indonesia.

Figure 2 .

 2 Figure 2. Aerial views of the landscapes at Weda Bay, Halmahera, Indonesia. Panel A shows exposed serpentinite bedrock in a rock fall near Jira with forest dominated by Casuarinaceae; panel B showing a riverbed upstream of the site of panel A with serpentinite bedrock and a short scrubby vegetation; Panel C shows mature riverine further downstream; panel D shows burnt vegetation on Plinthic Geric Rhodic Ferralsols near Uni-Uni.

Figure 3 .

 3 Figure 3. Ground-level views of vegetation types at Weda Bay, Halmahera, Indonesia. Panel A shows mature riverine forest at the site "Serpentinite River"; panel B shows mature forest near site Casuarina' panel C shows burnt 'maquis-type' vegetation characterised by sedges (Cyperaceae) on Geric Plinthic Rhodic Ferralsols at Uni-Uni, and panel D shows young forest dominated by Macaranga spp. (Euphorbiaceae) on Ferralic Rhodic Hypereutric Cambisols (Hypermagnesic) at Sake River.

Figure 4 .

 4 Figure 4. Soil profiles at key localities at Weda Bay, Halmahera, Indonesia. Panel A shows Hypereutric Cambic Skeletic Leptosols (Hypermagnesic) at the site "Blue Hill"; panel B shows Geric Plinthic Rhodic Ferralsols; panel C shows ferrocrete with plinthic nodules consisting mainly of hematite; panels D and E show Hypereutric Cambisols (Hypermagnesic) at the sites Casuarina and Sake West; panel F shows Geric Plinthic Rhodic Ferralsols at Uni-Uni.

Figure 5 .

 5 Figure 5. X-Ray Diffractograms of the fine earth fraction (< 50 mm) of the B horizons of 5 representative profiles on ultramafic bedrock and of the A-organo-mineral horizon of the Rendzic Leptosol on Limestone. CALC=Calcite; DIOP=Diopside; ENST=Enstatite; GIBBS=Gibbsite; GOET=Goethite; HEM=Hematite; MAGN=Magnetite; QUARTZ=Quartz; TREM=Tremolite; SERP=Serpentine.

Figure 6 .

 6 Figure 6. Plant part and soil total concentrations of different elements for nonhyperaccumulator plants (A) and hyperaccumulator plants (B). All concentrations are expressed as mg kg -1 dry mass.

Figure 8 .

 8 Figure 8. Plant foliar and soil bioavailable concentrations with DTPA extractions of different elements for non-hyperaccumulator plants and hyperaccumulator plants. All concentrations are expressed as mg kg -1 dry mass.

Figure 9 .

 9 Figure 9. The mistletoe Amyema cuernosensis parasitizing the Ni hyperaccumulator Ficus trachypison near the Casuarina site. Panel A shows the while mistletoe plant attached to the host; panel B shows the inflorescences of Amyema cuernosensis; and Panel C shows a section of woody stem of Ficus trachypison with the mistletoe stems attached with haustoria.

TABLE CAPTIONS Table 1 .

 CAPTIONS1 Sites properties showing plot enumeration, location, soil class and dominant vegetation type.

Table 11 .

 11 Elemental concentrations (mg kg -1 ) in the mistletoe Amyema cuernosensis

Primary minerals Clay minerals Iron oxides, Spinels and Al hydroxides Location Tremolite Diopside Enstatite Fayalite Palygorskite Calcite Quartz Smectite group clays Chlorite (clinochlore) Talc Serpentine Goethite Hematite Magnetite Gibbsi te

	Blue Hill		+	(+)		+	+++	(+)		+++	+	(+)	+
	Bukit Limber Plot 1					+			+	++ (clinochrys.)	+++	+	+
	Bukit Limber Plot 2								++		+++	(+)	+	+
	Casuarina Plot 1		+	+		++	++			++	+	++	++
	Casuarina Plot 2	+++				+	++	+	(+)	+	+	+
	Casuarina Plot 3					++					+++	+	++
	Doromesmesan Limestone Plot 1				+++	(+)
	Location 2A					+	+++	(+)		+	+	+	(+)
	Location 2B		++	+	+		+++	+	+
	Location 2C				(+)		+++
	Sake River						(+)			(+)	+++	+	+
	Sake South						(+)			+	+++	++	+
	Sake West					+			(+)		+++	+
	Uni-Uni plot 1									(+)	+++	+
	Uni-Uni plot 2						++			+++	+	++
	Woi Mioseng	+	+			+	+	(+)		+++	+	+	+

Table 2 .

 2 Mineralogy of the soils (Mineral horizons -10-25 cm layer) sampled at each site. For the soil in Doromesmesan, the mineralogy was based on the

	organo-mineral Horizon (0-5 cm layer). +++ (most abundant mineral); ++ (abundant mineral); + (frequent mineral); (+) (detectable traces).

Table 3 .

 3 Total elements for mineral soil (10-25 cm layer) samples from each site.

	10
	11

Table 4 .

 4 Total elements for organo-mineral soil (0-5 cm layer) samples from each site.

	14
	15

Table 5 .

 5 DTPA-extractable elements for mineral soil (10-25 cm layer) samples from each site.

	Location	Co (mg kg -1 )	Fe (mg kg -1 )	Mg (mg kg -1 )	Mn (mg kg -1 )	Ni (mg kg -1 )	Zn (mg kg -1 )
	Blue Hill	0.5	31	1 032	10	140	2.4
	Bukit Limber plot 1	0.7	18	352	7.2	24	0.6
	Bukit Limber plot 2	0.1	1 065	145	6.9	11	1.3
	Casuarina plot 1	2.7	147	1 176	33	375	9.4
	Casuarina plot 2	0.6	80	949	19	156	3.2
	Casuarina plot 3	15	42	209	55	518	11
	Doromesmesan Limestone Plot 1	0.6	20	196	35	6.0	2.2
	Location 2A	0.9	120	784	21	243	3.1
	Location 2B	0.1	5.7	593	7.4	0.1	0.2
	Location 2C	0.3	20	701	9.3	15	0.7
	Sake River	11	38	164	146	276	5.1
	Sake South	4.7	15	529	5.4	773	5.1
	Sake West	5.5	26	53	94	8.7	0.8
	Uni-Uni plot 1	2.2	38	13	145	12	1.1
	Uni-Uni plot 2	1.4	59	1 275	23	326	2.3
	Woi Mioseng	1.4	127	1 016	24	167	2.6

Table 6 .

 6 DTPA-extractable elements for organo-mineral soil (0-5 cm layer) samples from each site.

	Location	pH	CEC	K	Ca	Mg	Mn	Na	Ni	%N	%C	%Corg
			(cmol+ kg -1 )	(cmol+ kg -1 )	(cmol+ kg -1 )	(cmol+ kg -1 )	(cmol+ kg -1 )	(cmol+ kg -1 )	(cmol+ kg -1 )
	Blue Hill	7.30	33	0.09	12	50	0.01	0.07	0.12	0.09	1.5	1.6
	Bukit Limber plot 1	7.17	4.4	0.01	0.12	3.5	0.00	0.01	0.00	0.08	1.7	1.5
	Bukit Limber plot 2	5.31	2.1	0.08	0.03	0.13	0.01	0.04	0.01	0.36	6.0	5.3
	Casuarina plot 1	6.49	41	0.40	6.1	31	0.03	0.08	0.12	0.56	8.2	8.1
	Casuarina plot 2	6.23	23	0.21	5.7	25	0.14	0.09	0.06	0.37	5.9	6.7
	Casuarina plot 3	5.61	29	0.09	1.4	2.0	0.17	0.04	0.23	0.38	4.9	5.8
	Doromesmesan Limestone Plot 1 8.16	54	0.19	53	1.9	< LOD	0.12	< LOD 0.56	13	7.6
	Location 2A	6.86	38	0.17	13	21	0.02	0.08	0.10	0.55	7.3	6.9
	Location 2C	7.00	32	0.09	18	12	0.00	0.06	0.00	0.11	2.0	1.9
	Sake River	6.11	13	0.11	5.8	4.2	0.14	0.11	0.29	0.46	5.6	5.2
	Sake South	5.92	17	0.15	0.28	13	0.29	0.08	1.4	0.48	5.3	4.8
	Sake West	4.76	5.1	0.03	1.1	1.2	0.30	0.02	0.15	0.18	1.9	1.8
	Uni-Uni plot 1	4.07	2.0	0.05	0.17	0.07	0.24	0.01	0.01	0.36	4.5	4.2
	Uni-Uni plot 2	6.91	39	0.16	3.5	33	0.06	0.06	0.27	0.29	3.8	3.8
	Woi Mioseng	6.06	21	0.08	0.28	19	0.00	0.04	0.03	0.36	4.6	5.0
	< LOD: under the limit of detection

Table 7 .

 7 pH, exchangeable cations (cmol + kg -1 ) and nitrogen and carbon content for mineral soil (10-25 cm layer) samples from each site.Abbreviations: Cation Exchange Capacity (CEC), % of soil total nitrogen (%N), % of soil total carbon (%C), % of soil organic carbon (%Corg).

	Location	pH	CEC	K	Ca	Mg	Mn	Na	Ni	%N	%C	%Corg
			(cmol+ kg -1 )	(cmol+ kg -1 )	(cmol+ kg -1 )	(cmol+ kg -1 )	(cmol+ kg -1 )	(cmol+ kg -1 )	(cmol+ kg -1 )
	Blue Hill	7.10	39	0.18	18	22	0.01	0.06	0.01	0.43	7.9	5.2
	Bukit Limber plot 1	6.96	7.5	0.05	0.37	6.5	< LOD	0.01 < LOD 0.23	3.0	2.6
	Bukit Limber plot 2	4.65	5.2	1.2	1.8	4.1	0.21	0.57	0.06	1.7	35	33
	Casuarina plot 1	6.34	61	0.76	15	40	0.05	0.14	0.08	1.0	23	16
	Casuarina plot 2	6.78	45	0.42	12	27	0.06	0.09	0.05	0.53	9.4	9.3
	Casuarina plot 3	5.98	28	0.52	20	5.9	0.42	0.20	0.39	0.98	17	17
	Doromesmesan Limestone Plot 1 7.41	64	0.35	62	4.6	0.01	0.21 < LOD 0.98	22	16
	Location 2A	6.74	24	0.20	20	13	0.01	0.09	0.03	0.60	9.9	8.8
	Location 2B	6.90	28	0.01	18	9.8	0.01	0.35 < LOD 0.01	0.42	0.41
	Location 2C	8.07	45	0.20	35	14	0.01	0.06 < LOD 0.08	2.0	1.5
	Sake River	6.49	17	0.26	9.9	4.4	017	0.21	0.26	0.68	11	9.5
	Sake South	6.01	20	0.26	2.0	14	0.18	0.08	1.2	0.60	7.6	6.9
	Sake West	6.59	8.7	0.07	6.0	1.4	< LOD	0.02 < LOD 0.21	2.7	2.5
	Uni-Uni plot 1	5.77	4.3	0.03	2.9	0.38	0.21	0.01	0.01	0.38	6.5	5.8
	Uni-Uni plot 2	6.66	21	0.17	5.0	31	0.06	0.04	0.24	0.31	4.2	4.0
	Woi Mioseng	6.86	37	0.24	3.7	31	0.03	0.09	0.04	0.63	11	10
	< LOD: under the limit of detection

Table

Table

			Leaves	Mineral soils		Organic soils
			Hyperaccumulators Non-hyperaccumulators	Ni-DTPA (mg kg -1 )	Ni-CEC (cmol + kg -1 )	Ni-T (g kg -1 )	Ni-DTPA (mg kg -1 )	Ni-CEC (cmol + kg -1 )	Ni-T (g kg -1 )
		Blue Hill	n.d	375 (< LOD-2824)	75	0.012	3.5		0.001	3.4
		Bukit Limber plot 1	851	255 (< LOD-21439)	14	< LOD	4.4	24	< LOD	4.5
		Bukit Limber plot 2	n.d	8.7 (< LOD-95)	4.5	0.001	1.5	11	0.006	0.8
		Casuarina plot 1	11819 (1808-18636)	454 (< LOD-15904)	335	0.012	2.1		0.008	1.7
		Casuarina plot 2	10946 (10728-11163)	357 (< LOD-13762)	110	0.006	0.6		0.005	0.6
		Casuarina plot 3	6395 (1473-11317)	293 (< LOD-2473)	119	0.023	6.4		0.039	5.1
		Doromesmesan Limestone Plot 1	8.1	n.d	2.4	< LOD	0.3	6.0	< LOD	0.2
		Location 2A	15817	14 (< LOD-45)	158	0.010	2.3		0.003	2.1
		Location 2C	152	4.1 (< LOD-32)	25	< LOD	1.5	15	< LOD	1.2
		Sake River	1821 (215-5179)	351 (< LOD-3344)	208	0.029	9.8		0.026	8.4
		Sake South	3721 (25-22178)	955 (< LOD-15934)	704	0.144	14		0.119	12
		Sake West	815 (147-1203)	36 (< LOD-182)	17	0.015	8.2	8.7	< LOD	7.8
		Uni-Uni plot 1	6871 (986-11141)	587 (< LOD-7191)	4.0	0.001	5.5	12	0.001	5.7
		Uni-Uni plot 2	3917 (2825-5014)	409 (< LOD-12814)	267	0.027	4.6		0.024	4.9
		Woi Mioseng	6030 (1117-10943)	2.8 (< LOD-17)	107	0.003	2.0		0.004	1.8
	33	< LOD: under the limit of detection
	34	n.d.: no data
	35

ACKNOWLEDGEMENTS

We acknowledge the financial and operational support from Eramet and PT Weda Bay Nickel to conduct this research. The French National Research Agency through the national "Investissements d'avenir" program (ANR-10-LABX-21, LABEX RESSOURCES21) and through the ANR-14-CE04-0005 Project "Agromine" is acknowledged for funding support. PT Weda Bay Nickel were responsible for all relevant permits in Indonesia and for transporting the plant and soil samples for chemical analysis in France. A. van der Ent is the recipient of a Discovery Early Career Researcher Award (DE160100429) from the Australian Research Council.

SUPPLEMENTARY INFORMATION

Table S1. Macronutrients (g kg -1 ) of non-hyperaccumulator leaves (number of samples are indicated, means and ranges are provided). Table S2. Micronutrients (mg kg -1 ) of non-hyperaccumulator leaves (number of samples are indicated, means and ranges are provided).

Table S3. Macronutrients (g kg -1 ) of hyperaccumulator leaves (number of samples are indicated, means and ranges are provided).