Benjamin Barrois
email: benjamin.barrois@irisa.fr

Olivier Sentieys
email: olivier.sentieys@irisa.fr

Daniel Menard
email: dmenard@insa-rennes.fr

The Hidden Cost of Functional Approximation Against Careful Data Sizing -A Case Study

Many applications are error-resilient, allowing for the introduction of approximations in the calculations, as long as a certain accuracy target is met. Traditionally, fixed-point arithmetic is used to relax accuracy, by optimizing the bit-width. This arithmetic leads to important benefits in terms of delay, power and area. Lately, several hardware approximate operators were invented, seeking the same performance benefits. However, a fair comparison between the usage of this new class of operators and classical fixed-point arithmetic with careful truncation or rounding, has never been performed. In this paper, we first compare approximate and fixed-point arithmetic operators in terms of power, area and delay, as well as in terms of induced error, using many state-of-the-art metrics and by emphasizing the issue of data sizing. To perform this analysis, we developed a design exploration framework, APXPERF, which guarantees that all operators are compared using the same operating conditions. Moreover, operators are compared in several classical real-life applications leveraging relevant metrics. In this paper, we show that considering a large set of parameters, existing approximate adders and multipliers tend to be dominated by truncated or rounded fixed-point ones. For a given accuracy level and when considering the whole computation data-path, fixed-point operators are several orders of magnitude more accurate while spending less energy to execute the application. A conclusion of this study is that the entropy of careful sizing is always lower than approximate operators, since it require significantly less bits to be processed in the data-path and stored. Approximated data therefore always contain on average a greater amount of costly erroneous, useless information.

I. INTRODUCTION

Throughout its history, computing architectures have shown significant improvements in terms of performance and energy efficiency, mostly thanks to technology evolution forecast by Moore's law. However, in latest semiconductor technologies, energy efficiency is not scaling along with integration capacity since transistor and power budgets are no longer balanced with the end of Dennard's scaling. With the recent enthusiasm for the Internet of Things (IoT) and to reduce power consumption in High Performance Computing (HPC) systems, new ways of still improving energy efficiency must be found.

To face these limitations, research has to focus on computing architectures themselves and, especially on number representations and the way operations are computed. Choosing the right computation precision at the right time during the execution, while preserving the application functionality in reasonable bounds, is another promising approach for improving significantly energy efficiency. In many applications, numbers are represented using floating-point representation, which can reach a high level of accuracy regardless of the data dynamic range. However, this number representation presents an important overhead in terms of performance and energy. This cost can be overridden using fixed-point arithmetic, which represents fractional real numbers as integers. However, this fixed representation is less accurate and has to be managed by the programmer so the application respects a predefined accuracy target. This loss of accuracy is due to the necessity of dropping some bits during calculation, to avoid the use of big operators and to prevent computation from overflows.

This past decade, approximate computing has become a major field of research [START_REF] Xu | Approximate computing: A survey[END_REF] and a new kind of integer inexact operators emerged [START_REF] Lingamneni | Energy parsimonious circuit design through probabilistic pruning[END_REF]. Contrary to accurate, reduced-precision fixed-point operators, the operation result can possibly be false, with a certain quantity of error introduced depending on the inputs. Designing approximate operators explores a new tradeoff by intentionally introducing errors to improve performance and energy efficiency, and to overcome limitations of standard high-precision designs. Nevertheless, for a given accuracy target the benefits in terms of energy consumption of these approximate operators has not yet been fairly investigated in comparison to fixed-point arithmetic.

In this paper we propose a fair comparison between fixedpoint arithmetic relying on truncated or rounded accurate operators, and inexact operators. These two types of operators are compared in terms of energy consumption, delay, area cost, and computation accuracy with different error metrics. To broaden this comparison, several applications are considered. Finally, to perform this analysis, we developed a design exploration framework, which guarantees that all operators are compared using the same operating conditions.

The rest of the paper is organized as follows. Section II describes fixed-point arithmetic and approximate operators. The framework used for comparison is detailed in Section III. The comparison results for addition and multiplication operators are given in Section IV and for real applications in Section V before concluding in Section VI.

II. RELATED WORK

In this paper, all experiments are based on fixed-point arithmetic, meaning integers are used to represent fractional real numbers. On one side, accurate fixed-point operators are used and the data bit-width is adapted using truncation or rounding, thus generating computation errors. This bitwidth optimization is the only source of inaccuracy. On the other side, approximate operators are used. Their source of inaccuracy is the approximations they perform by design. This section presents the state of the art of fixed-point arithmetic and introduces the approximate operators used in this paper.

A. Fixed-Point Arithmetic

Fixed-point (FxP) arithmetic is widely used in low-power systems. This arithmetic uses basic integer operators and allows exploring the trade-off between accuracy and energy by adjusting the data bit-width. The fixed-point conversion aims at optimizing the data bit-width N to minimize the energy consumption. First the data dynamic range is determined to allocate the minimal number of bits m for the integer parts which guarantees no overflow. Then, the fractional part bit-width n is optimized to provide a minimal computation accuracy. A FxP real number x is approximated as an N -bit signed integer X scaled by a fixed factor, such as x = X.2 -n . The quantization process corresponding to the elimination of some bits of the n-bit fractional part leads to an unavoidable error. This error can be modelled by a uniformly distributed white noise [START_REF] Widrow | Statistical theory of quantization[END_REF]. The noise power is linked to the number of bits of the fractional part after the quantization process. By considering the classification proposed in [START_REF] Nogues | Algorithmic-level approximate computing applied to energy efficient hevc decoding[END_REF], quantization noise is a fail small error type i.e. the error has a high occurrence but with a small amplitude. In this paper, operators whose output is truncated (resp. rounded) will be denoted as OP t (resp. OP r ).

B. Approximate Hardware Operators

This study is performed using five state-of-the-art approximate operators -three adders and two multipliers. All were chosen for the good balance between their structural simplicity and their acceptable accuracy in comparison to other approximate operators, based on their claims and on literature. The three adders will be referred as ACA (Almost Correct Adder) [START_REF] Verma | Variable latency speculative addition: A new paradigm for arithmetic circuit design[END_REF], ETAIV (Error-Tolerant Adder type IV) [START_REF] Zhu | Enhanced low-power high-speed adder for error-tolerant application[END_REF] and RCAApx (Approximate Ripple-Carry-Adder) [START_REF] Gupta | Impact: Imprecise adders for low-power approximate computing[END_REF]. The two multipliers will be referred as AAM (Approximate Array Multiplier) [START_REF] Van | Design of the lower error fixed-width multiplier and its application[END_REF] and ABM (Approximate Booth Multiplier) [START_REF] Juang | Low-error carry-free fixed-width multipliers with low-cost compensation circuits[END_REF].

The structure of the three adders is schematized in Figure 1. Each input and output bit of the adders is represented by a black dot. A coloured rectangle on the inputs shows what bits are considered for computing the value of the output bits which are in a rectangle of same colour. A full line represents an accurate sum, while a dotted line represents an approximated addition, used only for RCAApx.

ACA [START_REF] Verma | Variable latency speculative addition: A new paradigm for arithmetic circuit design[END_REF] is probably the most classical and referenced inexact adder. ACA can be configured by its number of input bits N and the number of bits for its carry-in prediction P . Therefore, for each of each bit of rank i, the output is obtained by computing the accurate sum of a i a i-1 . . . a i-(P -1) a i-P and b i b i-1 . . . b i-(P -1) b i-P . ETAIV [START_REF] Zhu | Enhanced low-power high-speed adder for error-tolerant application[END_REF] is the result of a series of improvements of ETAII [START_REF] Zhu | An enhanced low-power highspeed adder for error-tolerant application[END_REF]. It is configured by N and the number of bits per block X. Indeed, ETAIV is divided into N/X blocks of size X. Each of these blocks performs the accurate sum of a N -kX-1 . . . a N -(k+1)X and b N -kX-1 . . . b N -(k+1)X , taking an input carry generated considering the outputs of the two previous blocks. RCAApx [START_REF] Gupta | Impact: Imprecise adders for low-power approximate computing[END_REF] is very different from the two others since it relies on the approximation of the full-adder (FA) logic. It is composed of two parts: the MSB part, which is an accurate adder, and the LSB part composed by the approximate FA. Three types of approximate FA can be used, as defined in [START_REF] Gupta | Impact: Imprecise adders for low-power approximate computing[END_REF]. RCAApx can be configured by N , the number of output bits computed using an accurate adder M , and the type of approximate FA used F AT ype (1, 2 or 3 sorted by decreasing accuracy). The first multiplier to be presented here is AAM [START_REF] Van | Design of the lower error fixed-width multiplier and its application[END_REF]. It is based on a fixed-width accurate array multiplier, which means that N × N input bits result in N output bits instead of 2N . To obtain AAM, half of the array multiplier basic cells are pruned above its first diagonal (in the classical representation of an array multiplier) and a compensation is performed using a simple series of AND and OR gates along this diagonal.

+ (a) Accurate adder -N = 8 + (b) ACA -N = 8, P = 2 + (c) ETAIV -N = 8, X = 2 + (d) RCAApx -N = 8, M = 3
ABM [START_REF] Juang | Low-error carry-free fixed-width multipliers with low-cost compensation circuits[END_REF] is a Radix-2 pruned Modified-Booth (MB) encoding-based multiplier. Radix-2 MB encoding uses one of the input as a coder for the addition grid, allowing a division by 2 of its size. Therefore, the area and delay of the resulting multiplier are improved, despite an overhead for the coder and the decoder which is necessary to convert the output from a redundant to a two's complement representation. However, redundant representation can be advantageously used to perform further calculation, hence the overhead of the decoder can be neglected. ABM approximates the multiplication by pruning half of the summand grid, with a compensation circuit using the most significant bits of the dropped part.

These approximate operators leads to output error compared to the exact value for some input values. These error have a low occurrence but can have a high amplitude. Errors associated with approximate operators are in the fail rare and fail moderate error type [START_REF] Nogues | Algorithmic-level approximate computing applied to energy efficient hevc decoding[END_REF].

III. AUTOMATED COMPARISON FRAMEWORK

In this section, we define the framework developed to compare fixed-point and approximate operators. We also define the error metrics used for accuracy evaluation. The proposed automated framework APXPERF, depicted in Figure 2, performs a totally automated characterization of a given operator and uses VHDL and C/C++ operator descriptions. APXPERF framework will be soon delivered as open-source.

HDL Simulation C Simulation

Veri¡cation

Data Fusion

Operator HDL Description

RTL Synthesis

Gate-Level Sim.

Power Estimation

Random Inputs

Operator C/C++ Code Func. Simulation

Extraction of Error Metrics

Performance and Error Metrics Results

Fig. 2: APXPERF framework To compare approximate arithmetic operators in a fair way, the operators are all generated and tested using the same constraints and conditions. An arithmetic operator is specified mainly at the register-transfer level (RTL), with some structure details sometimes expressed at the gate level. From this specification, delay constraints, and any technology library, APXPERF generates detailed delay, area, and power results for the operator, using a three-step design flow. First, RTL synthesis is used to obtain an optimized gate-level netlist as well as area and timing information. Second, the gatelevel description is simulated using a customizable number of random inputs to generate an activity file. Finally, an analysis is performed using this file and the technology library to estimate power consumption.

In parallel, a functional characterization of the given operator is performed, using its C/C++ description. After an automated validation of the VHDL and C file equivalence, an important number of error metrics are extracted from the operator, using a customizable number of random inputs, leveraging OpenMP simulation acceleration using computing clusters. Then, hardware and functional generated results are gathered and saved as a Matlab MAT file. Matlab functions and scripts are provided to browse and process these results.

Several kinds of error metrics must be considered to characterize operators. Indeed, depending on the application the operator is supposed to be used in, different metrics can be representative of its accuracy. For instance, metrics taking the significance of each bit into consideration can be used in a signal processing application, whereas other metrics would fit better for an application for which any bit position has the same significance, such as most data compression algorithms.

The error e = x -x is the difference between the approximate and exact integer outputs. x k is the k-th bit of the N -bit integer x. In this paper, Mean Square Error (MSE) E e 2 and Bit Error Rate (BER)

[x -x = 0], positional BER E [x k ⊕ x k ]
for all bit position k, Acceptance Probability (AP) given several values of Minimum Acceptable Accuracy (MAA) [START_REF] Zhu | Design of low-power high-speed truncation-error-tolerant adder and its application in dsp[END_REF], Probability Density Function (PDF), and Power Spectral Density (PSD) of error e.

IV. RAW RELATIVE PERFORMANCE ANALYSIS

A first comparison of fixed-point and approximate operators consists in comparing the accuracy of each of them regarding a performance metric (energy, area, delay). For this, all approximate operators of Section II-B were compiled and tested with a number of bits varying from 2 to 32 and all possible combination of parameters. FxP operators (i.e. classical integer adders and multipliers) were tested in the same way, with all possible combinations of input and output size (inputs from 2 to 32, outputs from 2 to 32 for the adders and 2 to 64 for the multipliers). All power results are given for a clock frequency of 100 MHz. The resulting files and useful graphs are generated using APXPERF. Design Compiler (2013.03) was used for RTL synthesis with a 28nm FDSOI technology library, Modelsim (10.3c) for gate-level simulation and PrimeTime (2013.12) for power analysis. Simulation and power analysis are performed on 10 5 random input samples. The extraction of error metrics based on the C description was computed on more than 10 7 random inputs.

- In some applications, all output bits have the same weight on the error. Therefore results on BER metric are presented on Figure 4 for the same adders than previously. Approximate operators achieve very good BER performance when compared to fixed-point operators. Considering the power and area, truncated and RCAApx adders perform similarly for any fixed BER. However, for delay and energy per addition, most approximate operators perform significantly better truncated or rounded FxP operators. When not considering bit significance in the operands, FxP operators are penalized by the suppression of part of their output bits, implicitly forcing them to zero.

Results for the multipliers are presented in Table I. The 16 to 32 integer multiplier is considered as the correct multiplier for accuracy reference. As AAM and ABM multipliers are fixed-width operators (16-bit inputs and output), comparison results are provided only for the truncated FxP multiplier with 16-bit output (MUL t (16, 16)). Fixed-width MUL t truncated multiplier reaches the best accuracy, and consumes least power. Although MUL t is slower than ABM, its energy per multiplication (PDP) is 44% better than both approximate operators. ABM is 37% faster than MUL t and AAM is 17% smaller. However, ABM is extremely MSE inaccurate, with 7 orders of magnitude more erroneous results than fixed-point. Both AAM and ABM are worse than MUL t by about 19% for BER metric.

As a conclusion for this operator-level performance analysis of various approximation schemes, fixed-point operators perform better when considering the MSE metric representative of signal processing applications, while approximate adders show good BER performance. However, the importance of output bit-width was not taken into account in this results. Indeed, when the bit-width is reduced, as in truncated or rounded operators, the amount of data to transfer to load and store operator inputs and output is consequently reduced. This shortening in bit-width has a major impact on energy consumption and must be considered for real-life application. Thus, although inexact and truncated-or-rounded operators seem to reveal the same gross performance, selecting the second one will allow to decrease energy cost by avoiding the transfer and memory storage of useless erroneous bits.

V. APPLICATION-BASED COMPARISON

In this section, the effect of fixed-point and approximate adders and multipliers is evaluated on different real-life applications, leveraging relevant and adapted metrics. Considered applications include Fast Fourier Transform (FFT), JPEG image encoder, motion compensation filtering in the context of High-Efficiency Video Coding (HEVC) decoding, and Kmeans clustering.

A. Fast Fourier Transform

As a classical computation kernel used in many signal processing or communication applications, FFT is relevant for this study. APXPERF provides an instrumented, tunable FFT kernel. This sections presents results on a 32-sample Radix-2 FFT computed on 16-bit input/output data. In a first experiment, only the adders are considered. The total energy to compute the FFT is estimated by

P DPF F T = N add i=1 P DP add,i + N mul i=1 P DP mul,i (1)
where N add and N mul are the total of additions and multiplications, respectively. Figure 5 shows P DP F F T as a function of output Peak Signal-to-Noise Ratio (PSNR). PSNR is the maximal power of the output signal divided by the MSE, i.e., P SN R(x) [dB] = 10. log max(x 2 ) M SE(x) . The exact multipliers used alongside the modified adders are optimally sized according to the adder bit-width, so they are not source of error. For any accuracy constraint, FxP adders (truncation or rounding) notably dominate approximate adders. This supremacy could be explained by two factors: the relative energy cost of multipliers with regards to adders and the need for less operand size for the multiplier when reducing the accuracy of additions. This figure also shows the great potential of energy reduction when playing with accuracy of the fixedpoint operators. A first conclusion here is that reducing the FxP adder size provides a smaller entropy of the data processed, transported and stored, than keeping the same bitwidth along the computations but containing approximations. The same experiment is performed using 16-bit AAM and

B. JPEG Encoding

The second application is a JPEG encoder, representative of image processing. The main algorithm of this encoder is the Discrete Cosine Transform (DCT). To obtain an approximate version of the encoder, DCT operations are computed using fixed-point or approximate operators. The quality metric to compare the exact and the approximate versions of the JPEG encoder is the Mean Structural Similarity (MSSIM) [START_REF] Wang | Image quality assessment: from error visibility to structural similarity[END_REF], which is representative of the human perception of image degradation. This metric results in a score between [0, 1], 1 representing a perfect quality. To obtain Figure 6, the DCT energy consumption is compared for all presented approximate adders, as well as for fixed-point versions. The algorithm is applied with an encoding effort of 90% on the image Lena. As observed for the FFT, the fixed-point versions of the algorithm are much more energy efficient than for approximate operators, mostly thanks to the bits dropped during the calculation. HEVC is the new generation of video compression standard. Efficient prediction of a block from the others requires fractional position motion compensation (MC) carried-out by interpolation filters. These MC filters are modified using fixedpoint and approximate operators to test their accuracy and energy efficiency. Previously described MSSIM metric is used to determine the output accuracy of the filter on a classical signal processing image. Table III gives the energy spent by the MC filter replacing all its additions by adders producing an MSSIM of approximately 0.99. In their 16-bit version, ACA and ETAIV can only reach respectively 0.96 and 0.98. In any case and as discussed above, the multiplier overhead provokes an energy consumption which is 4.6 times superior for the approximate version than for the truncated FxP version. For multipliers replacement, Table III shows that both 16-bit AAM and ABM produce an accuracy similar to fixed-width truncated FxP multiplier. Moreover, replacing multipliers by ABM in the MC filter do not lead to an important energy overhead, which makes it competitive considering that its delay is 37% inferior to MUL t (16, 16) according to Table I. However, AAM suffers from an important energy overhead.

D. K-means Clustering

The last experiment presented in this section is K-means clustering. Given a bidimensional point cloud, this algorithm classifies them finding centroids and assigning each point to the cluster defined by the nearest centroid. At the core of Kmeans clustering is distance computation. For the experiment, In spite of the theoretical competitiveness of approximate operators, their advantages are likely to be lost at application level. Indeed, at the difference of fixed-point operators, accuracy reduction is obtained by simplifying the operator structure but not by reducing the operator output bit-width. This reduces the energy of the considered operator, but does not have a positive impact on the other operators, as for fixed-point.

VI. CONCLUSION

In this paper, two types of hardware approximation were compared: fixed-point arithmetic relying on truncated and rounded accurate operators with careful data sizing, and approximate operators. A direct comparison using the APX-PERF framework showed that both techniques are competitive, depending on the observed error and performance metrics. However, stepping back observing some state-of-the-art applications showed that using approximate operators often leads to an important overhead since they manipulate larger data containing in average more erroneous useless information bits. More generally, it has been shown that comparing the raw performance of operators does not necessarily reflect their performance in a given application context. Hence, a major stake for hardware approximation is now to be considered at a higher level to take more parameters into consideration. An effort must also be made in the research for more efficient approximate multipliers, since they are responsible for the majority of power consumption in computation-intensive applications. However, considering approximate operators in embedded processors to replace or enhance their integer arithmetic unit would still be a good option, since processor data size is fixed and cannot be application specific.

Fig. 1 :

 1 Fig. 1: Structure of the considered approximate adders

Fig. 5 :

 5 Fig.5: Power consumption of FFT-32 versus output PSNR using 16-bit approximate adders ABM multipliers and a 16-bit truncated FxP multiplier, while keeping 16-bit exact adders. TableIIshows that AAM and FxP multiplier differ only by 6 dB of of accuracy. However, AAM consumes 78% more energy that fixed-point. Results on the FFT comfort the conclusion of Section IV. Providing results with both approximate adders and multipliers in the same simulation will not lead to a different conclusion.

  trunc. Fixed-Point round.

Fig. 6 :

 6 Fig. 6: Power consumption of DCT in JPEG encoding versus output MSSIM using 16-bit approximate adders C. Motion Compensation filter for HEVC decoder

  Mean Average Error (MAE) E [|e|], less penalizing than MSE for high amplitude errors, relative error E x-x x , inferior and superior bound of error (min e , max e ), error rate P

	1 N E

N k=0

x k ⊕ x k are considered for accuracy metrics. To provide detailed information for each type of application, APXPERF moreover embeds the following metrics: mean error (or error bias) µ e = E [e],

TABLE I

 I

	: Direct comparison of 16-bit-input and output fixed-
	point and approximate multipliers
	(PDP). For the sake of clarity, results are here only presented
	for 16-bit input operators. 16-bit output is considered as the
	correct adder and used as reference. Truncated and rounded
	FxP adder outputs vary from 15 to 2 bits (from left to right).
	For approximate adders, results are given by varying: the
	number of approximated LSBs (M ) and types of FA for
	RCAApx, the maximal size of carry chain (P ) for ACA, and
	the block size (X) for ETAIV. What can be first noticed is
	that in terms of power consumption and design area, fixed-
	point operators are better than approximate operators for a
	same MSE, except for very-low accuracy. However, in terms
	of delay, most approximate operators are faster, but they cannot
	reach the same level of accuracy when more than 8 bits are
	kept for the fixed-point output. In terms of energy, the PDP
	of FxP adders is quite near from approximate ones when less
	than 8 output bits are kept. However, ACA and RCAApx are
	able to spend less energy without sacrificing much accuracy.

  TableIIshows that AAM and FxP multiplier differ only by 6 dB of of accuracy. However, AAM consumes 78% more energy that fixed-point. Results on the FFT comfort the conclusion of Section IV. Providing results with both approximate adders and multipliers in the same simulation will not lead to a different conclusion.

		MULt (16, 16) AAM (16) ABM (16)
	PSNR (dB)	53.88	59.66	-18.14
	PDP (pJ)	0.249	0.442	0.446

TABLE II

 II

	: Accuracy and energy consumption of FFT-32 using
	16-bit fixed-width multipliers

TABLE III :

 III Accuracy and energy consumption of distance computation for HEVC Filter using 16-bit input adders

		MSSIM	Multiplier Energy (pJ) Energy (pJ) Min. Adder	Total Energy (pJ)
	MULt(16, 16) 99.918%	2.49E-1	1.83E-2	3.77
	AAM(16)	99.909%	4.42E-1	1.83E-2	6.48
	ABM(16)	99.907%	2.54E-1	1.83E-2	3.85

TABLE IV :

 IV Accuracy and energy consumption of distance computation for HEVC using 16-bit input multipliers 5 sets of 5E3 points of data were generated around 10 random points with a Gaussian distribution. The accuracy metric is the success rate, from 0 to 1, representing the proportion of points classified in the correct cluster. Table V presents the success rate and energy spent in distance computation replacing the exact adders by fixed-point and approximate versions. For truncated fixed-point version, the energy spent in multiplication is inherently inferior to approximate, thanks to the reduction of bit-width, leading to a total energy reduction by more than half for a success rate of 99%, and even by nearly 10 for a success rate of about 86%. TableVI

		Success	Adder	Min. Mult.	Total
		Rate	Energy (pJ) Energy (pJ) Energy (pJ)
	ADDt(16, 11)	99.14%	1.55E-2	9.36E-2	2.03E-1
	ACA(16, 12)	99.10%	1.54E-2	2.49E-1	5.13E-1
	ETAIV(16, 4)	99.43%	1.30E-2	2.49E-1	5.11E-1
	RCA Apx (16, 6, 3)	99.67%	1.00E-2	2.49E-1	5.08E-1
	ADDt(16, 8)	86.00%	1.27E-2	2.40E-2	6.06E-2
	ACA(16, 8)	86.06%	9.85E-3	2.49E-1	5.08E-1
	ETAIV(16, 2)	63.25%	7.00E-3	2.49E-1	5.05E-1
	RCA Apx (16, 10, 1) 87.29%	1.26E-2	2.49E-1	5.11E-1

TABLE V :

 V Accuracy and energy of distance computation for K-means using 16-bit input adders for different success rates shows K-means clustering success rate and energy spent in distance computation performing multiplication using 16-bit input FxP and approximate multipliers. AAM achieves similar accuracy than fixed-width truncated accurate multiplier, with 99% success rate. However, it presents an energy overhead of 75%. ABM achieves very poor performance for K-means, with only 10% success, which is equivalent to prune 12 output bits of a FxP multiplier.

		Success	Multiplier	Min. Adder	Total
		Rate	Energy (pJ) Energy (pJ)	Energy (pJ)
	MULt(16, 16) 99.84%	2.49E-1	1.83E-2	5.15E-1
	AAM(16)	99.43%	4.42E-1	1.83E-2	9.02E-1
	ABM(16)	10.27%	2.54E-1	1.83E-2	5.27E-1
	MULt(16, 4)	10.87%	2.04E-1	1.24E-3	4.09E-1

TABLE VI :

 VI Accuracy and energy of distance computation for K-means using 16-bit input multipliers


Magali Lucia
email: magali.lucia@npolar.no

Hallvard Strøm

Paco Bustamante

Geir W Gabrielsen

Trace Element Concentrations in Relation to the Trophic Behaviour of Endangered Ivory Gulls (Pagophila eburnea) During Their Stay at a Breeding Site in Svalbard

Keywords: Ivory gull, Seabird, Mercury, Metal, Arctic, Stable Isotopes

The ivory gull is a high-Arctic species considered endangered in most parts of its breeding range. Ivory gulls must cope with both the reduction of sea ice cover triggered by climate change and increasing contaminant loads due to changes in global contaminant pathways. The objective of this study was to assess the concentration of 14 essential and non-essential trace elements at four colonies of ivory gulls breeding on Barentsøya, Svalbard, and the relationship between contaminant exposure and the diet of individuals. Contaminants and stable isotopes (δ 15 N, δ 13 C) were determined in blood (red blood cells and whole blood), and feathers of ivory gulls collected over several years. The most quantitatively abundant non-essential trace element found in the ivory gull was mercury (Hg). Selenium (Se) was present in substantial surplus compared with Hg, which would imply relative protection against Hg toxic effects but raises concern about Se potential toxicity. Moreover, other elements were detected, such as silver, arsenic, cadmium, and lead, which would warrant monitoring because of the potential additive/synergetic effects of these compounds. This study demonstrated individual differences in trophic behaviour that triggered discrepancies in Hg concentrations, highlighting the potential biomagnifying ability of this metal in the ivory gull's food web. Results highlighted the mixing of birds coming from different geographical areas on Barentsøya.

Introduction

Among trace elements, some are categorized as non-essential, such as silver (Ag), cadmium (Cd), lead (Pb), and mercury (Hg), whereas others are considered nutritionally essential, such as arsenic (As), cobalt (Co), chromium (Cr), copper (Cu), iron (Fe), manganese (Mn), nickel (Ni), selenium (Se), vanadium (V), and zinc (Zn). However essential, all of these trace elements can become toxic at high exposure levels.

Seabirds can bioaccumulate high contaminant levels due to their wide distribution, long life-span, and high position in the food chain [START_REF] Hobson | A stable isotope (δ 13 C, δ 15 N) model for the North Water food web: implications for evaluating trophodynamics and the flow of energy and contaminants[END_REF]. These top-predators are affected by biomagnification processes of a variety of elements (e.g., Hg) with concentrations consistently increasing from lower to higher trophic levels where several studies observed sublethal and/or lethal concentrations and adverse effects [START_REF] Gibson | A positive correlation between mercury and oxidative stress-related gene expression (GPX3 and GSTM3) is measured in female Double-crested Cormorant blood[END_REF]Goutte et al. 2014a, b). One of the main goals in ecotoxicology is to examine more precisely the trophic ecology of species to better understand exposure pathways and explain contaminant concentrations in animal populations. In this context, carbon and nitrogen stable isotopes have become a powerful tool to investigate trophic relationships and/or origins of prey to elucidate broad-scale, inter-, and intraspecific dietary patterns. Consequently, studies in this field allow investigating whether differences in foraging strategies can explain variations in contaminant uptake [START_REF] Jardine | Applications, considerations, and sources of uncertainty when using stable isotope analysis in ecotoxicology[END_REF].

The ivory gull (Pagophila eburnea) is a high-Arctic species spending the entire year in the north closely associated with sea ice. Three main wintering grounds were identified for northeast Atlantic populations (north Greenland, Svalbard, and Franz Josef Land) of this long distant migrant species in southeast Greenland, along the Labrador sea-ice edge and the Bering Strait region [START_REF] Gilg | Postbreeding movements of northeast Atlantic ivory gull Pagophila eburnea populations[END_REF]Spencer et al. 2014). The species is listed as ''Near Threatened'' by the International Union for Conservation of Nature and considered endangered in most part of its breeding range. This ivory gull is especially endangered in Canada, where numbers have declined by 80-85 % since the 1980s [START_REF] Gilchrist | Declines in abundance and distribution of the ivory gull (Pagophila eburnea) in Arctic Canada[END_REF]. Nevertheless, it is one of the world's most poorly known species even though its high position in the marine food web makes it sensitive to contaminant exposure [START_REF] Karnovsky | Distribution and diet of ivory gulls (Pagophila eburnea) in the North Water Polynya[END_REF]. The ivory gull is indeed known to feed mainly on polar cods (Boreogadus saida) and crustaceans associated with the ice edge or to scavenge remains of polar bear kills [START_REF] Mehlum | Seabird distribution in the northern Barents Sea marginal ice-zone during late summer[END_REF][START_REF] Mehlum | The diet of High-Arctic seabirds in coastal and ice-covered, pelagic areas near the Svalbard archipelago[END_REF][START_REF] Karnovsky | Distribution and diet of ivory gulls (Pagophila eburnea) in the North Water Polynya[END_REF]. [START_REF] Bond | Rapidly increasing methyl mercury in endangered ivory gull (Pagophila eburnea) feathers over a 130 year record[END_REF] suggested that the population decline observed in the Canadian Arctic may be linked partly to declines in reproduction success from increased exposure to Hg and its methylated form (MeHg).

Previous studies also demonstrated high exposure to organic contaminants along the distribution range of the ivory gull [START_REF] Braune | Levels and trends of organochlorines and brominated flame retardants in Ivory Gull eggs from the Canadian Arctic, 1976 to 2004[END_REF][START_REF] Miljeteig | High levels of contaminants in ivory gull Pagophila eburnea eggs from the Russian and Norwegian Arctic[END_REF][START_REF] Lucia | Circumpolar contamination in eggs of the high-Arctic ivory gull Pagophila eburnea[END_REF]. However, apart from Hg, nothing is known about the exposure to trace elements of this free-ranging Arctic species.

The purpose of the present study was to examine concentrations of essential and non-essential trace elements (Ag, As, Cd, Co, Cr, Cu, Fe, Hg, Mn, Ni, Pb, Se, V, and Zn) at four colonies of ivory gulls breeding on Barentsøya, Svalbard, and the relationship between contaminant exposure and the diet of individuals. Trace elements were determined in blood (red blood cells or whole blood depending on the year) and ventral feathers of ivory gulls collected between 2011 and 2014. In parallel, carbon and nitrogen stable isotopes were determined on the same tissues to investigate the foraging ecology during both breeding and moulting periods, which are greatly overlapping in the ivory gull presumably due to the constraints of its high-latitude winter range and the brief Arctic summer [START_REF] Howell | Molt of the Ivory Gull[END_REF]. In this species, adults have only a single moult per cycle. Nevertheless, exposure and diets between breeding and moulting can be dissociated due to the fact that the moult is mostly completed before the prelaying to hatching period (mid June to early August).

Materials and methods

Sample collection and preparation

Ivory gulls were collected for blood and ventral feathers between 2011 and 2014 at four breeding colonies (Auga, Freemanbreen, Hübnerbreen, Sigden, Fig. 1) on Barentsøya, Svalbard, and along the ice edge in Spring (April). Birds were caught by the use of a single-catch closing net trap baited with a small piece of seal blubber. Blood was sampled from the brachial vein. When it was possible, sex was determined through DNA analysis, as well as morphometric measurements (e.g., mass).

Overall, whole blood was sampled for isotope analyses and trace element determination in 2011 (n = 6), 2012 (n = 4), and 2013 (n = 5), whereas red blood cells (erythrocytes) were obtained after centrifugation in the field (4000 rpm, 10 min) in 2013 (n = 40) and 2014 (n = 42). Ventral feathers were sampled in 2011 (n = 19), 2012 (n = 40), 2013 (n = 47), and 2014 (n = 39). Over the years, red blood cells were sampled in four colonies: Auga (n = 5), Freemanbreen (n = 24), Hübnerbreen (n = 20), Sigden (n = 28), whole blood in two colonies: Freemanbreen (n = 7), Hübnerbreen (n = 2), and the ice edge (n = 5), and feathers in four colonies: Auga (n = 5), Freemanbreen (n = 70), Hübnerbreen (n = 31), Sigden (n = 30), and the ice edge (n = 8). All the blood samples were stored at -20 °C until further analyses. Blood samples were later freeze-dried, then grounded and stored in individual plastic vials until further trace element and isotopic analyses. Ventral feathers were washed to remove oil and dirt in a chloroform-methanol solution (2:1) in an ultrasonic bath for 2 min. Afterwards, they were rinsed in two consecutive pure methanol baths for a few seconds and dried at 40 °C for 48 h.

Trace element determination

Analyses were performed at the UMR 7266 CNRS Université de La Rochelle in France. Total Hg analyses were performed with an Advanced Mercury Analyser (ALTEC AMA 254), on dried tissue aliquots ranging from 1 to 20 mg, weighed to the nearest 0.01 mg. For Hg determination, the metal was evaporated by progressive heating up to 800 °C, then held under oxygen atmosphere for 3 min, and finally amalgamated on a gold net. Afterwards, the net was heated to liberate the collected Hg, which was measured by atomic absorption spectrophotometry. Mercury analyses were run according to a thorough quality control program, including the analysis of a NRC reference material (lobster hepatopancreas TORT-2; National Research Council, Canada). Standard aliquots were treated and analysed according to the same conditions as the samples. Results were in good agreement with certified values, with a mean recovery rate of 98 %. The detection limit was 5 ng Hg g -1 dry weight (dw).

Ag, As, Cd, Co, Cr, Cu, Fe, Mn, Ni, Pb, Se, V, and Zn were analysed using a Varian Vista-Pro ICP-OES and a ThermoFisherScientific XSeries 2 ICP-MS. Aliquots of the biological samples (20-200 mg) were digested with 6 ml 67-70 % HNO3 and 2 ml 34-37 % HCl (Fisher Scientific, trace element grade quality) (except for feathers: 3 ml HNO3 and 1 ml HCl). Acidic digestion of samples was performed overnight at room temperature, then using a Milestone microwave (30 min with constantly increasing temperature up to 120 °C, then 15 min at this maximal temperature). Each sample was completed to 50 ml (or 25 ml for feathers) with milli-Q water. Three control samples (two Certified Reference Materials, CRMs, and one blank) treated and analysed in the same way as the samples were included in each analytical batch. CRMs were dogfish liver DOLT-4 (NRCC) and lobster hepatopancreas TORT-2 (NRCC). Quantification limits and mean recovery rates were, respectively, equal to 0.1 µg L -1 and 77% for Ag, 1 µg L -1 and 96% for As, 0.1 µg L -1 and 100% for Cd, 0.1 µg L -1 and 98% for Co, 0.1 µg L -1 and 97% for Cr, 0.5 µg L -1 and 94% for Cu, 20 µg L -1 and 90% for Fe, 0.5 µg L -1 and 91% for Mn, 0.2 µg L -1 and 98% for Ni, 0.1 µg L -1 and 94% for Pb, 0.5 µg L -1 and 97% for Se, 2 µg L -1 and 97% for V, and 20 µg L -1 and 102% for Zn. Trace element concentrations are expressed in µg g -1 dw.

Nitrogen and carbon stable isotope analysis

Depending on birds and years, stable isotopes were determined in ventral feathers and, either on the whole blood or red blood cells (see above). Analyses were performed at the UMR 7266 CNRS-Université de La Rochelle in France. Cleaned feathers of ivory gulls were finely chopped using stainless steel surgical scissors and accurately weighed (± 0.001 mg) to a range between 0.1 and 0.4 mg. Blood samples were also weighed with the same accuracy and in the same range of masses.

All samples were placed in tin capsules for carbon and nitrogen stable isotope analysis and analysed using an elemental analyser (Flash EA 1112 fitted with a "No Blank" option, Thermo Scientific, Milan, Italy) coupled to an isotope ratio mass spectrometer (Delta V Advantage, Conflo IV interface, Smart EA option, Thermo Scientific, Bremen, Germany). Results are reported in δ unit notation (expressed in per mil relative to standards: Vienna Pee Dee Belemnite for δ 13 C and N2 in air for δ 15 N). The analytical precision of the measurements was < 0.06 ‰ and < 0.1 ‰ for carbon and nitrogen, respectively.

Data treatment and statistical analyses

Several compounds that were detected or analysed in less than 60% of the samples were excluded from statistical analyses including As, Cr, and V for feathers, Ag, Co, Cr, Ni and V for red blood cells, and Ag, Cd, Co, Cr, Ni, V for the whole blood. Values below the quantification limit were taken into account in calculation of the means by assigning those values one-half of the detection limit for the given contaminant (e.g. a value < 0.02 ng g -1 dw was reported as 0.01 ng g -1 dw).

As normality and homogeneity of variance were not achieved despite log10(x+1) transformation (Cochran C test), non-parametric analysis of variance (Kruskal-Wallis and Mann-Whitney U-test) was applied to assess differences in contaminant concentrations for each parameters (e.g. tissue, colony, year, sex). Moreover, the Spearman test was applied to all correlations achieved in this study.

Principal Component Analysis (PCA) was used to identify trends in the distribution of trace element concentrations among individuals collected. Each trace element concentration was first normalized (mean was subtracted and the difference was then divided by the standard deviation).

Four separate analyses were performed to investigate the distribution of individuals in regards of two factors: the year and the colony, and using in both cases feather and red blood cell data. These analyses were performed using the PERMANOVA + package [START_REF] Anderson | PERMANOVA + for PRIMER: Guide to software and statistical methods[END_REF] from PRIMER v6 [START_REF] Clarke | The pelagic feeding habits of ivory and Ross' gulls[END_REF].

Results

Trace element concentrations in tissues

Mean concentrations and ranges of the 14 trace elements in feathers, whole blood and red blood cells of the ivory gull are presented in Tables 1 and2 for non-essential and essential elements, respectively. In general, trace element concentrations strongly varied between tissues. Most nonessential element concentrations were low, especially for Ag, Cd and Pb (Table 1). Concentrations in feathers were however mainly above detection limits. Mercury reached high mean concentrations, ranging between 0.81 ± 0.05 µg g -1 dw in the whole blood and 3.39 ± 0.30 µg g -1 dw in feathers. In the latter tissue, Hg concentrations ranged between 0.41 and 14.8 µg g -1 dw, and 13% of the individuals displayed concentrations above 5 µg g -1 dw. Differences between tissues were analysed taking into account birds which have been sampled for both blood and feathers. All year combined, Hg concentrations in the blood were significantly lower than in feathers (Mann-Whitney test, p < 0.01). Concentrations of Cd were also significantly higher in feathers compared to red blood cells (Mann-Whitney test, p < 0.001). In parallel, Cd concentrations in both tissues were positively correlated (r = 0.49; Spearman correlation test, p < 0.05). Lead concentrations, however, were higher in red blood cells due to the high levels reached in 2014 (0.70 ± 0.13 µg g -1 dw). To exclude year as confounding factor, red blood cells and feathers were compared in 2013 only. Lead concentrations in red blood cells were subsequently lower than in feathers (p < 0.001).

Similarly, Pb concentrations in the whole blood, determined between 2011 and 2013, were lower than in feathers (Mann-Whitney test, p < 0.001). Lead concentrations in feathers and red blood cells were, as for Cd, positively correlated (r = 0.47; Spearman correlation test, p < 0.05). Finally, no correlations were observed between feathers and whole blood concentrations for all the elements studied.

For essential trace elements, Co, Cr and Ni concentrations were low in all tissues (Table 2).

Vanadium was always below quantification limits. Arsenic in feathers was also below quantification limits, whereas higher mean concentrations were found in the blood. Mean concentrations were indeed comprised between 3.76 ± 0.56 µg g -1 dw in the whole blood in 2011 and 5.27 ± 0.60 µg g -1 dw in red blood cells in 2013. Two other elements, Fe and Se, displayed higher blood concentrations than in feathers (Table 2). Both elements had however their feather concentrations positively and significantly correlated to their respective blood concentrations (Fe: r = 0.41, Se: r = 0.53; Spearman correlation test, p < 0.05). Conversely, Cu concentrations were significantly higher in feathers than in blood. Depending on the year, mean feather concentrations ranged between 16.5 ± 0.39 and 17.9 ± 0.35 µg g -1 dw, whereas mean whole blood and red blood cell concentrations were comprised between 0.99 ± 0.02 µg g -1 dw and 1.21 ± 0.05 µg g -1 dw. The same pattern was observed for Mn and Zn, which displayed significantly higher concentrations in feathers (Mann-Whitney test, p < 0.05).

Numerous correlations were found between elements in all tissues (Table 3). Correlations between trace element concentrations appeared however to vary in regard of tissues, especially for feathers and red blood cells where the highest number of individuals were studied. Among the relationships between trace elements, Cu and Fe were positively correlated in feathers (r = 0.25) but negatively in red blood cells (r = -0.51). Iron also was negatively correlated to Pb in red blood cells (r = 0.46). Mercury and Se were positively correlated in both feathers and red blood cells (r = 0.22, r = 0.28, respectively; Table 3). The Se:Hg molar ratios were calculated in tissues of ivory gulls. The ratios always exceeded 1 for all the birds in the blood and ranged between 14 and 139.

Ratios in feathers were considerably lower and ranged between 0.3 and 6.7.

Influence of the year, colony, sex, and body weight on trace element concentrations

Several trace elements showed an increasing trend over the years (Tables 1 and2). In feathers, this trend was observed for Ag, Cd in 2014, and even Mn and Se between 2011 and 2013. However, Mn and Se concentrations also demonstrated a decrease in 2014. In red blood cells, even if the data only represent two years of sampling, an increase in concentrations could be observed for Cd, Cu and Pb between 2013 and 2014. Figure 2 presents PCAs performed on ivory gull data in feathers and red blood cells to identify trends in the distribution of trace elements between years. For feathers, the first 2 axes extracted 36.4% of the variance of the data clouds (Figure 2A). The first axis (PC1) was positively correlated with Co, Fe and Mn, whereas the second axis (PC2) was positively correlated with Cd, Hg and Se concentrations (Figure 2A). The projection of feather samples demonstrated that ivory gulls sampled in 2013 were characterized by slightly higher Co, Fe, and Mn concentrations. However, this trend only appeared for part of the birds sampled that year. Overall, differences between years were unclear in this tissue. Conversely, a PCA was performed with red blood cell data, even if this tissue was only collected in 2013 and 2014 (Figure 2B). The first axis (PC1) was positively correlated with Fe and negatively with Cu and Pb, whereas the second axis (PC2) was negatively correlated with Cd, Mn and Zn concentrations. The projection of red blood cell samples demonstrated a clear dichotomy between 2013 and 2014, both years being separated along the first axis even if individuals belonging to both years were scattered across the PCA. In 2013, birds were characterized by higher As, Fe, Hg and Se concentrations, whereas in 2014, birds displayed higher Cu and Pb concentrations. No PCA was realized on whole blood data because of the few birds sampled for this tissue.

Figure 3 presents PCAs performed on ivory gull data in feathers and red blood cells to identify trends in the distribution of trace elements between colonies and the ice edge. For feathers, the first 2 axes extracted 36.7% of the variance of the data clouds (Figure 3A). Overall, no clear tendencies and differences were observed between colonies. Another PCA was realized with red blood cell data (Figure 3B). The first axis (PC1) was negatively correlated with Cu and Pb, whereas the second axis (PC2) was positively linked with Mn and Zn. Most of the birds were spread across the PCA with, as in feathers, unclear trends. Nevertheless, it should be noted that birds from Sigden, even if scattered across the graph, showed a tendency of higher Cu and Pb concentrations than in other colonies. Indeed, mean Cu concentration in Sigden reached 1.13 ± 0.03 µg g -1 dw, and was significantly higher than in Auga (0.95 ± 0.01 µg g -1 dw) and Hübnerbreen (1.00 ± 0.02 µg g -1 dw; Kruskal-Wallis test, p < 0.05), but not than in Freemanbreen (1.03 ± 0.02 µg g -1 dw). For Pb, Sigden concentration (0.75 ± 0.17 µg g -1 dw) was significantly higher than both Hübnerbreen (0.07 ± 0.04 µg g -1 dw) and Freemanbreen (0.22 ± 0.11 µg g -1 dw; Kruskal-Wallis test, p < 0.05), but not significantly different to Auga (0.38 ± 0.21 µg g -1 dw).

The sex of ivory gulls was successfully determined in 24 females and 65 males for feather samples, and 18 females and 30 males for red blood cell samples. The influence of sex was then investigated on both tissue concentrations. For the most part, no differences were observed between females and males. Even if differences were low, females displayed significantly higher Ag concentrations than male in feathers (female: 0.065 ± 0.004 vs male: 0.055 ± 0.002 µg g -1 dw; Mann-Whitney test, p = 0.042), and both Mn (female: 0.15 ± 0.01 vs male: 0.13 ± 0.01 µg g -1 dw; p = 0.023) and Zn (female: 21.9 ± 0.3 vs male: 21.2 ± 0.3 µg g -1 dw; p = 0.033) in red blood cells.

Finally, the relation between trace element concentrations and total body weight of birds was investigated. The body weight of ivory gulls was positively correlated with Hg concentrations in red blood cells (r = 0.28), and negatively with Mn concentrations in the whole blood (r = -0.63; Spearman correlation test, p < 0.05). No correlations appeared between feather concentrations and body weight of birds.

Relationship between trophic position, feeding habitat and trace element concentrations

The relation between the trophic behaviour, assessed through the determination of δ 15 N and δ 13 C, and trace element concentrations of ivory gulls was studied in three tissues: feathers, red blood cells and whole blood. Of all elements, Hg was positively correlated with δ 15 N and δ 13 C in all tissues, with the exception of δ 15 N in the whole blood (δ 15 N: rfeathers = 0.36, rred blood cells = 0.46; δ 13 C: rfeathers = 0.51, rred blood cells = 0.50, rwhole blood = 0.52; Spearman correlation test, p < 0.05; Figure 4).

Figure 4 showed that one individual for both feathers and red blood cells presented high Hg and stable isotopes levels. These individuals, corresponding to two different birds for both tissues, could be identified as mostly responsible for the positive correlations observed. However, those correlations still appeared when these individuals were removed from analyses (data not shown).

In red blood cells, other relationships were significant, such as positive correlations between δ 13 C and both Fe (r = 0.40) and Se (r = 0.25) concentrations, as well as negative correlations between δ 13 C and Cd (r = -0.32), Cu (r = -0.29), and Pb (r = -0.35) concentrations. In feathers, δ 13 C was negatively linked with Ag (r = -0.29), whereas δ 15 N was negatively correlated with Ni (r = -0.21).

Finally, in the whole blood, the only correlations observed apart from Hg, were between δ 15 N and both Mn (r = 0.54) and Se (r = -0.60).

Discussion

Trace element concentrations and toxicology significance

Although most trace elements occur naturally in the marine environment, they also are widely released through anthropogenic activities. Even if few of these activities are located in the Arctic, this region acts as a sink for contaminant produced in industrialized parts of the world and transported northward by air, sea, and water masses [START_REF] Poissant | Critical review of mercury fates and contamination in the arctic tundra ecosystem[END_REF]. Moreover, in a changing environment, the Arctic is likely to be submitted to increasing anthropogenic pressure. As of today, few studies have focused on trace elements in Arctic seabirds [START_REF] Braune | Trace element and metallothionein concentrations in seabirds from the Canadian Arctic[END_REF][START_REF] Øverjordet | Effect of diet, location and sampling year on bioaccumulation of mercury, selenium and cadmium in pelagic feeding seabirds in Svalbard[END_REF]. The present study allowed investigating trace element concentrations in one of the most poorly researched seabirds in the Northern hemisphere: the ivory gull. Overall, most of the elements studied were detected in this species, even if low elemental concentrations were mainly recorded.

Among elements with the highest levels, Hg is one of greatest concern in the Arctic environment because of its capacity to undergo long-range atmospheric transport and be deposited northwards.

Polar regions act as sinks for Hg [START_REF] Macdonald | Recent climate change in the Arctic and its impact on contaminant pathways and interpretation of temporal trend data[END_REF]. Melting snow and ice allow the transfer of Hg to the marine environment and its biomagnification up the food chain [START_REF] Campbell | Mercury and other trace elements in a pelagic Arctic marine food web (Northwater Polynya, Baffin Bay)[END_REF]).

In the ivory gull, [START_REF] Bond | Rapidly increasing methyl mercury in endangered ivory gull (Pagophila eburnea) feathers over a 130 year record[END_REF] demonstrated a clear increase in feather MeHg concentrations between 1877 and 2007 using museum specimens from the Canadian Arctic and western Greenland (from 0.09 to 4.11 µg g -1 in adults). These authors also reported total Hg concentrations reaching on average 3.84 ± 2.02 µg g -1 in post-1975 years. Previous reports from studies examining the Arctic have shown an east-west increase of Hg egg concentrations of the ivory gull [START_REF] Lucia | Circumpolar contamination in eggs of the high-Arctic ivory gull Pagophila eburnea[END_REF]. Those higher Hg concentrations in the Canadian Arctic were partly explained by naturally higher Hg levels in sediments from this region associated with the deposition of large amounts of anthropogenic Hg that originated from China [START_REF] Muir | Spatial and temporal trends and effects of contaminants in the Canadian Arctic marine ecosystem: A review[END_REF]AMAP 2011). In the present study, ivory gull from Svalbard indeed displayed slightly lower concentrations than in the Canadian Arctic and western Greenland [START_REF] Bond | Rapidly increasing methyl mercury in endangered ivory gull (Pagophila eburnea) feathers over a 130 year record[END_REF], reaching 3.39 ± 0.30 µg g -1 in feathers in 2014. This concentration also was well below observed levels in ivory gull feathers collected in 2010 on Seymour Island, Canada, where the concentration was on average 11.66 ± 5.52 µg g -1 dw.

However, some individuals in the present study reached high Hg concentrations, exceeding 5 µg g -1 dw in feathers, threshold that would be indicative of body burdens of Hg that would have adverse effects (Burger and Gochfeld 1997a). Mercury is mainly accumulated as MeHg in feathers (Thompson and Furness 1989). [START_REF] Mallory | Mercury concentrations in feathers of marine birds in Arctic Canada[END_REF] found that MeHg averaged 67-81 % of the total Hg in ivory gull feathers from the Canadian Arctic. Overall, these results suggest that Hg concentrations may be sufficiently elevated to trigger sublethal effects and/or reproduction impairments and consequently contribute to the population decline [START_REF] Burgess | Methylmercury exposure associated with reduced productivity in common loons[END_REF][START_REF] Bond | Rapidly increasing methyl mercury in endangered ivory gull (Pagophila eburnea) feathers over a 130 year record[END_REF]. Nevertheless, Hg toxicity often is balanced by Se accumulation and the formation of Hg-Se complexes. Both element concentrations were positively correlated in feathers and red blood cells of ivory gulls. Selenium is essential to organisms' metabolism but can also be toxic depending upon the chemical form ingested (Stewart et al. 1999). Both elements' chemical properties have therefore a key role in alleviating their respective toxicity at high exposure [START_REF] Khan | Mercury-selenium compounds and their toxicological significance: towards a molecular understanding of the mercury-selenium antagonism[END_REF]. Mercury and Se were found to be positively linked in both feathers and red blood cells. Selenium toxic effects include reproductive impairments with teratogenesis, growth reduction, histopathological lesions, alterations in hepatic glutathione metabolism, and even direct mortality in some cases [START_REF] Hoffman | Role of selenium toxicity and oxidative stress in aquatic birds[END_REF]. In blood samples of this study, Se was present in a substantial surplus compared with Hg. Feather Se:Hg ratio was on average 1.45 ± 0.08, therefore suggesting the presence of mercuric selenide, a well-known non-toxic form in marine mammals and birds [START_REF] Ikemoto | Detoxification mechanism of heavy metals in marine mammals and seabirds: interaction of selenium with mercury, silver, copper, zinc, and cadmium in liver[END_REF][START_REF] Khan | Mercury-selenium compounds and their toxicological significance: towards a molecular understanding of the mercury-selenium antagonism[END_REF]. Overall, ivory gulls are presumably protected against Hg toxicity, but those results raise concern about Se toxicity to this species.

Another interesting result was the detection of other trace elements, such as Ag (feathers), As (blood), Cd, and Pb. Although low emissions of Cd were recorded in the Arctic, other studies have found Cd bioaccumulation in Arctic seabirds (Øverjordet et al. 2015). The global anthropogenic emission of Cd exceeded natural emissions in the mid-1980s (AMAP 1997). However, Cd presence in the Arctic is thought to be linked to geochemical processes of the ocean and, therefore, mainly originating from natural emissions. Little evidence was found about Cd in marine systems being impacted by human activities [START_REF] Macdonald | Contaminants in the Canadian Arctic: 5 years of progress in understanding sources, occurrence and pathways[END_REF]. Lead presence in the Arctic is of concern because of the long-range transport of this metal. Lead has been delivered in large amounts to the Arctic and is thought to mainly come from industrial activities [START_REF] Pacyna | The origin of Arctic air pollutants: lessons learned and future research[END_REF][START_REF] Macdonald | Contaminants in the Canadian Arctic: 5 years of progress in understanding sources, occurrence and pathways[END_REF]. Even though Ag, Cd, and Pb were encountered at low levels, it should be noted that both Ag and Cd in feathers, as well as Pb in the blood, had a tendency to increase between 2013 and 2014. Of course, these data only represent 2 years of sampling and efforts should be made to extend that time frame. Nevertheless, the detection of these elements and the increasing pattern should raise concern about the transport of these metals to the Arctic environment and potential consequences for sensitive species, such as the ivory gull, that are spending their life span in Northern environments. Those species will have to cope with not only the reduction of sea ice cover triggered by climate change but also increasing contaminant loads due to changes in global contaminant pathways and new anthropogenic pressures [START_REF] Macdonald | Recent climate change in the Arctic and its impact on contaminant pathways and interpretation of temporal trend data[END_REF]. Conversely to these metals, As reached relatively high levels in blood samples of ivory gulls. Background As concentrations are usually low in living organisms (<1 µg g -1 wet weight (ww), approximately 5 µg g -1 dw; [START_REF] Eisler | Arsenic hazards to fish, wildlife, and invertebrates: A synoptic review. Contaminant Hazard Reviews Report No. 12[END_REF]. Reference values for blood As in birds from uncontaminated areas is approximately 0.02 µg g -1 ww (approximately 0.4 µg g -1 dw in red blood cells; Burger and Gochfeld 1997b;[START_REF] Anderson | Element patterns in albatrosses and petrels: Influence of trophic position, foraging range, and prey type[END_REF]. For the ivory gull, As concentrations in red blood cells and whole blood were well above those levels, reaching 3.98 ± 1.45 µg g -1 dw and 5.27 ± 0.60 µg g -1 dw, in 2012 for the whole blood and 2013 for red blood cells, respectively. Arsenic may act as an endocrine disruptor, impair reproduction, trigger sublethal effects or even induce individuals' death in acute cases of As poisoning [START_REF] Eisler | A review of arsenic hazards to plants and animals with emphasis on fishery and wildlife resources[END_REF][START_REF] Kunito | Arsenic in marine mammals, seabirds, and sea turtles[END_REF]). Nevertheless, this element is considered mainly toxic under its inorganic form. In marine biota, As mainly occurs as arsenobetaine, a water soluble organoarsenical that poses little risk to organisms or their consumers. Some ivory gulls specialise on scavenging remains of polar bear kills, whereas others feed on polar cod and crustaceans associated with the ice edge. The importance of polar cods to the diet of ivory gulls has been documented [START_REF] Clarke | The pelagic feeding habits of ivory and Ross' gulls[END_REF][START_REF] Mehlum | Seabird distribution in the northern Barents Sea marginal ice-zone during late summer[END_REF][START_REF] Mehlum | The diet of High-Arctic seabirds in coastal and ice-covered, pelagic areas near the Svalbard archipelago[END_REF][START_REF] Karnovsky | Distribution and diet of ivory gulls (Pagophila eburnea) in the North Water Polynya[END_REF]. [START_REF] Sele | A study of lipid-and water-soluble arsenic species in liver of Northeast Arctic cod (Gadus morhua) containing high levels of total arsenic[END_REF] studied lipid-and water-soluble As species in livers of Northeast Arctic cods (Gadus morhua). Cods with high total As concentrations contained 3 to 7 % of the total As in the lipid-soluble fraction containing several arsenolipids. Arsenic was therefore mainly present in the water-soluble fraction as arsenobetaine. In contrast, cods displaying low As concentrations contained up to 50 % of the total As as lipid-soluble species. Knowledge about lipid-soluble species is still limited in terms of distribution, metabolism, and also toxicity.

Nevertheless, it is very much probable that ivory gulls mainly ingest As under its arsenobetaine form when feeding on polar cods, therefore implying little toxicity for the birds. Overall, it appears however evident that the cumulative and synergetic effects of trace elements, associated with already high organic contaminant levels previously recorded, could be detrimental to this endangered species [START_REF] Braune | Elevated mercury levels in a declining population of ivory gulls in the Canadian Arctic[END_REF][START_REF] Lucia | Circumpolar contamination in eggs of the high-Arctic ivory gull Pagophila eburnea[END_REF].

Relationship between trophic position, feeding habitat and trace element concentrations

Food is the main pathway of contaminant exposure for seabirds. Ivory gulls tend to occupy a high trophic position in the Arctic food web year-round and, consequently, are exposed to high contaminant levels, especially through biomagnification processes [START_REF] Hobson | Extending an indicator: year-round information on seabird trophic ecology from multiple-tissue stable-isotope analyses[END_REF].

Stable isotope analyses have become a powerful tool to study dietary exposure and biomagnification of contaminants in free-ranging animal populations [START_REF] Jardine | Applications, considerations, and sources of uncertainty when using stable isotope analysis in ecotoxicology[END_REF]). In the present study, both nitrogen and carbon values of birds were positively correlated to Hg concentrations in most of the tissues. Ivory gulls feeding at higher trophic position, and on more inshore prey enriched in 13 C were more likely to display high Hg exposure and concentrations. The current study demonstrated that individual differences in trophic behaviour triggered discrepancies in Hg concentrations and the potential biomagnifying ability of this metal in the ivory gull's food web. Mercury under its methylated form is indeed well known for its ability to biomagnify in the Arctic pelagic food web [START_REF] Ruus | Methylmercury biomagnification in an Arctic pelagic food web[END_REF]. Conversely, Ni and Se concentrations, in feathers and whole blood, respectively, demonstrated negative relationships with δ 15 N. Such relationships have been previously demonstrated for Ni in the muscle of seabirds [START_REF] Campbell | Mercury and other trace elements in a pelagic Arctic marine food web (Northwater Polynya, Baffin Bay)[END_REF].

Biomagnification of Se, however, has been reported by some authors [START_REF] Lemly | Selenium transport and bioaccumulation in aquatic systems: a proposal for water quality criteria based on hydrological units[END_REF][START_REF] Muscatello | Selenium accumulation in aquatic biota downstream of a uranium mining and milling operation[END_REF], whereas others reported no relationship with trophic position (Barceloux 1999;[START_REF] Campbell | Mercury and other trace elements in a pelagic Arctic marine food web (Northwater Polynya, Baffin Bay)[END_REF][START_REF] Lucia | Trace element accumulation in relation to trophic niches of shorebirds using intertidal mudflats[END_REF]. Results of the present study tend to indicate trophically decreasing Se concentrations along the ivory gull's food web.

Stable carbon values (δ 13 C) vary little along the food chain. In the marine environment, δ 13 C values are mainly used to determine foraging habitats of predators [START_REF] Rubenstein | From birds to butterflies: animal movement patterns and stable isotopes[END_REF]. Carbon values of ivory gulls were negatively correlated to several elements, including Cd, Cu, and Pb in red blood cells, as well as Ag in feathers. This result highlighted that birds feeding on prey enriched in 13 C were consequently less likely to have high Ag, Cd, Cu, and Pb concentrations. The inverse pattern has been observed for Fe and Se in red blood cells.

Finally, most of the colonies sampled showed similar stable isotope values and trace element levels, especially in feathers, which are a record of exposure during their formation. This pattern could be explained by two main factors. First, birds from Barentsøya are coming from large areas and travel wide distances to reach their breeding sites. These birds can consequently, at their arrival on their breeding ground, mix between themselves, which would partly explain similarities between colonies, especially in feathers. Conversely, this mixing is creating individual differences in isotopic values and trace element levels within each colony. Second, colonies sampled on Barentsøya are geographically close to each other. Distances are limited and birds from those colonies are most probably using similar feeding grounds around the island and along the ice edge.

Nevertheless, it should be noted that birds from the Sigden colony, even if individual variability occurred, showed a tendency of higher Cu and Pb concentrations in red blood cells compared with other colonies.

A previous study on the ivory gull found that birds from Sigden displayed significantly different isotopic values in red blood cells compared with other colonies on Barentsøya [START_REF] Lucia | Contamination of ivory gulls (Pagophila eburnea) at four colonies in Svalbard in relation to their trophic behavior[END_REF].

Birds from Sigden had lower δ 13 C values. As stated, Cu concentrations were negatively linked to δ 13 C values. The trophic behaviour of Sigden birds might explain contaminant variability found in this study. This result should be considered with caution and may be a snapshot of contaminant exposure and trophic behaviour during an episodic event (e.g., climatic event, poor sea-ice conditions). More data are needed to envision whether differences persist in time in the context of a changing Arctic environment.

Conclusion

The most quantitatively abundant, non-essential trace element found in the ivory gull was Hg. In blood samples, Se was present in a substantial surplus compared to Hg. Even though ivory gulls were presumably protected against Hg toxicity, this study raised concern about Se toxicity in this sensitive species. Moreover, other trace elements were detected, such as Ag, As, Cd, and Pb, which would warrant monitoring because of their potential additive/synergetic effects. The current study demonstrated both individual differences in trophic behaviour that triggered discrepancies in Hg concentrations, and the biomagnifying ability of this metal in the ivory gull's food web. This study also highlighted the mixing of birds coming from different geographical areas on Barentsøya, which would partly explain similarities between colonies in terms of isotopic values, trace element levels, and overall individual variability within each colony. Finally, more data are needed to understand fully the ivory gull's trophic behaviour and its link with trace element levels, especially in the context of a changing environment. Table 1 Concentrations (Mean ± SD, range; µg g -1 dw) of non-essential trace elements in tissues of the ivory gull (Pagophila eburnea)

from Barentsøya (Svalbard) in 2011[START_REF] Hobson | Extending an indicator: year-round information on seabird trophic ecology from multiple-tissue stable-isotope analyses[END_REF][START_REF] Lucia | Trace element accumulation in relation to trophic niches of shorebirds using intertidal mudflats[END_REF], 2014 nd: values below the detection limit Significant differences between years for each trace element and tissue distinctly are indicated by letters at the level α = 0.05 (Mann-Whitney U-test)

Table 2 Concentrations (Mean ± SD, range; µg g -1 dw) of essential trace elements in tissues of the ivory gull (Pagophila eburnea) from Barentsøya, Svalbard, in 2011[START_REF] Hobson | Extending an indicator: year-round information on seabird trophic ecology from multiple-tissue stable-isotope analyses[END_REF][START_REF] Lucia | Trace element accumulation in relation to trophic niches of shorebirds using intertidal mudflats[END_REF], 2014 nd: between 60% and 100% of the values were below the quantification limit, therefore, no means were calculated. When all values were below the quantification limit, "nd" was also indicated in range boxes Significant differences between years for each trace element and tissue distinctly are indicated by letters at the level α = 0.05 (Mann-Whitney U-test)

Fig. 1 Fig. 3 Fig. 4

 134 Fig. 1 Locations of four ivory gull (Pagophila eburnea) colonies sampled on Barentsøya (78°25'N, 21°27'E), Svalbard, Norway

Table 3

 3 Correlation between trace elements in feathers, whole blood, and red blood cells of the ivory gull (p < 0.05; Spearman correlation test)

	Elements	Feathers	Whole blood	Red blood cells
	Ag	+Cd, +Cu
	As		-Pb	-Mn, -Pb
	Cd	+Ag, +Hg, +Se		+Cu, -Fe
	Co	+Cu, +Fe, +Mn, +Ni, +Pb, -Zn
	Cr
	Cu	+Ag, +Co, +Fe, +Mn, +Se		+Cd, -Fe, +Pb
	Fe	+Co, +Cu, +Mn, -Zn	+Pb	-Cd, -Cu, -Pb, +Se
	Hg	+Cd, -Ni, +Se	+Zn	+Se
	Mn	+Co, +Cu, +Fe, +Ni, +Pb, -Zn		-As
	Ni	+Co, -Hg, +Mn, -Zn
	Pb	+Co, +Mn	-As, +Fe	-As, +Cu, -Fe
	Se	+Cd, +Cu, +Hg		+Fe, +Hg
	Zn	-Co, -Fe, -Mn, -Ni	+Hg

Acknowledgments. Funding was provided by Seventh Framework Programme (Grant no. 622019). The authors thank the European Commission for its financial support through a Marie Curie fellowship to M. Lucia, as well as Gael Guillou from the plateforme ''Analyses Isotopiques'' of LIENSs for technical support during isotopic analyses. We thank Carine Churlaud and Maud Brault-Favrou from the plateforme ''Analyses Elémentaires'' of LIENSs for their assistance with chemical analyses. The CPER (Contrat de Projet Etat-Région) is acknowledged for the funding of the ICP and AMA. The fieldwork was supported by the Norwegian Polar Institute's centre for Ice, Climate and Ecosystems (ICE), and the SEAPOP program (seapop. no). Thanks to Vidar Bakken, Audun Igesund, Cecilie Miljeteig, Knut Olsen, Maria Gavrilo, Olivier Gilg, and Odd Kindberg for help in the field.

Spencer NC, Gilchrist HG, Mallory ML (2014)