Towards on-chip time-resolved thermal mapping with micro-/nanosensor arrays

Haixiao Liu
Weiqiang Sun
An Xiang
Tuanwei Shi
Qing Chen
Shengyong Xu
Towards on-chip time-resolved thermal mapping with micro-/nanosensor arrays
N A N O E X P R E S SReal-time thermal mappingSensor arrayThin-film thermocoupleNanoscale thermometryOn-chip hot spot detection
In recent years, thin-film thermocouple (TFTC) array emerged as a versatile candidate in micro-/nanoscale local temperature sensing for its high resolution, passive working mode, and easy fabrication. However, some key issues need to be taken into consideration before real instrumentation and industrial applications of TFTC array. In this work, we will demonstrate that TFTC array can be highly scalable from micrometers to nanometers and that there are potential applications of TFTC array in integrated circuits, including time-resolvable two-dimensional thermal mapping and tracing the heat source of a device. Some potential problems and relevant solutions from a view of industrial applications will be discussed in terms of material selection, multiplexer reading, pattern designing, and cold-junction compensation. We show that the TFTC array is a powerful tool for research fields such as chip thermal management, lab-on-a-chip, and other novel electrical, optical, or thermal devices.

Background

One of the major bottlenecks of fast development in the modern electronics industry is heat. Managing the high heat flux generated by billions of transistors in an integrated circuit (IC) is the main challenge. A scalable, builtin, and agile temperature sensor which can provide realtime thermal history of an IC chip is essential to thermal failure analysis [1]. However, thermal measurement at microscale and nanoscale is a technical challenge. When both high spatial resolution and high temperature sensitivity are required, only a few approaches, such as scanning thermal microscopy [2], luminescent nanoparticles, and infrared thermography [3][4][5], remain in the list of suitable candidates. If built-in thermal sensors are required for time-resolvable solutions in a solid device, such as in IC chips, micro-electro-mechanical system, a lab-on-a-chip, or a flexible printed circuits, then it seems that only stripe-shaped resistive sensor [6] and thin-film thermocouple (TFTC) are left in the candidate list. The passive nature of a thermocouple makes it superior to a resistive thermal sensor (usually made of metal or semiconductors) because a thermocouple provides a far more rapid response, does not require external excitation voltage or current, and generates no additional heat which may cause unexpected electrical noise and error in temperature measurement.

A TFTC works on a well-known Seebeck effect [7], i.e., a thermoelectric voltage will be generated when a temperature difference is established between two ends of a conductor. The ability to generate thermoelectric signal was symbolized by the Seebeck coefficient (S). A TFTC is made when two different conductors α and β join together at one end (hot end). If there is a temperature difference (ΔT), then a thermoelectric voltage (ΔV) can be collected at the open end (usually kept cold, referred as the cold end) as follows:
ΔV ¼ S α À S β À Á Á T h À T c ð Þ¼TP Á ΔT;ð1Þ
where S α and S β represent the Seebeck coefficients of α and β, and T h and T c are the temperatures at the hot end and cold end, respectively. TP means the thermopower of thermocouple, which is the sensitivity of the sensor. Given the measured ΔV, T c , and TP, one can easily calculate the T h . By embedding thermocouples in an electrical device, e.g., an IC chip, one can monitor the temperature at the area of thermocouple junction even after packaging. In addition, the measured voltage signal is just relative to the temperature of the junction area; thus, by shrinking the junction area of the thermocouple, one can obtain a highly localized temperature measurement. Pioneering work on scaling down the size of a TFTC has pushed its junction area to 100 × 100 nm [8], suggesting the potential for local temperature sensing at the nanoscale. Finally, the fabrication process for a TFTC is compatible with the welldeveloped microelectronic techniques. As a result, TFTCs have attracted much attention in recent years [9][10][11][12][13][14][15].

In 2005, Park et al. firstly constructed 100 TFTCs into an array providing two-dimensional (2D) temperature mapping in an area of around a square centimeter [12]. A few years later, Grayson et al. discussed some considerations in the progress of instrument TFTC array into real IC chips [13,14]. Recently, we presented a novel method for time-resolved 2D mapping by TFTC array [15] and firstly constructed a functional TFTC array made of a single material [16]. As a built-in solution, TFTC array is gaining more and more attention. However, to further push forward the development of TFTC array and its instrumentation in electronics industry, more potential advantages have to be explored, and some related issues have to be addressed.

In this work, we report on our recent work on TFTC array, including construction of the first nanoscale TFTC array in an area of 5 × 5 μm. We demonstrate that besides real-time temperature mapping, the TFTC array can also be utilized in mapping time-resolved heat flux and tracing a possible hot spot on a surface. We also discuss some key issues of instrumentation in IC chips in the future, including choice of material, multiplexing, pattern designing, and cold end problems.

Methods

Material selection

Semiconductor-based thermocouples play an important role in industries on thermal sensing because of their high Seebeck coefficients, which are usually 20 to 500 times higher than metal-based thermocouples. Thus, thermocouples based on silicon, germanium, tellurium, or semiconductor compounds were often adopted in occasions that required high sensitivity; see Table 1 [17,18]. Applicationspecific chips like infrared radiation detection were frequently reported [19][20][21], where high dependency between output signal and the heat induced by incident infrared radiation was preferable. The semiconductor-based thermocouples were connected in series as a thermopile to provide larger output signals, typically 10 V/W. However, in ordinary temperature measuring situations, semiconductor-based TFTCs were not selected extensively. From Table 1, we can find very low figure of merit (ZT) in all these materials, which means that they can hardly be ideal materials in thermoelectric applications like cooling or power generation with high efficiency. If n-type and p-type materials with high figure of merit (ZT % 3) can really be synthesized in the future, thermoelectric pairs made by these materials can probably function as chip coolers or micro-power generators with the temperature measuring at the same time. As only for thermal measurement, the Seebeck coefficient is our main concern, and the figure of merit is not so critical. We choose Cr and Ni as TFTC composition materials. The Cr-Ni TFTCs 100-nm thick provide TP of around 26.2 ± 1.5 μV/K stably [15], which is large enough to provide a temperature resolution better than 0.1 K. Typical Cr-Ni TFTC characterization data are presented in Figure 1, where the negligible hysteresis in heating and cooling processes indicates the reliability.

Moreover, unlike the intrinsic Seebeck coefficient of metals, the Seebeck coefficient of semiconductor is highly extrinsic in relevance with the doping density, crystal structure, and resistivity. For example, the Seebeck coefficient of p-type silicon varied from 300 to 1,600 μV/K at room Table 1 Typical physical properties and figure of merits of candidate materials (300 K)
Materials S (μV/K) ρ (Ω m) κ (W/m K) ZT Cr 18.8 1.27E − 7 93.9 8.9E − 3 Ni −18 7E − 8 90.9 1.5E − 2 Al −1.7 2.65E − 8 237 1.4E − 4 Si a Approximately −450 1.4 132 3.3E − 7 poly-Si a Approximately −1,200 0.36 135 8.9E − 6 n-poly-Si b −57 8.1E − 6 31.5 3.8E − 3 p-poly-Si b 103 2.2E − 5 31.2 4.6E − 3 n-poly-SiGe b −77 2.4E − 5 9.4 7.9E − 3 p-poly-SiGe b 59 1.9E − 5 11.1 5.0E − 3 a
The samples of Si and poly-Si have intrinsic N-type impurities [17]; b the doping concentration was 2.5E20 atoms/cm 3 [18].

Figure 1

The TP is calculated from the slope of the plot.

temperature [22]. Because of its relevance to fabrication process, the thermopower of semiconductor-based thermocouple may vary from batch to batch or even from one to another, which was hard to put into industrial batch productions. As for the metal-based thermocouples, they were put into wide applications for many years, and industrial standard thermocouples were all made of metals or alloys. Thin-film metal thermocouple can generate a similar thermopower given similar film thicknesses. Varrenti et al. first reported the reproducibility of Cr-Ni TFTCs, both interand intra-batch [14]. Our work also contributed to the high stability of Cr-Ni TFTCs by massive calibrations [15].

As to the fabrication, Cr-Ni TFTCs can also be produced in CMOS-compatible processes just like the silicon-based temperature sensors. The differences were that sputtering was used in metal fabrications, and diffusion or ion implantation was adopted in doped silicon stripe fabrication. Si-based thermocouple fabrication may require additional lithography and etching to remove the superfluous undoped silicon to avoid short circuit. Besides, metals can be incorporated in different layers of ICs. The silicon-based device always synthesized in the same layer of the ICs, consuming precious spaces.

Array designing and multiplexing

Previously reported TFTC arrays were all constructed in an area larger than 5 × 5 mm [12,13,15]; we show that the size, density, and pattern of a TFTC array can be far more flexible. Using standard industrial processes of photo lithography, e-beam lithography, and thin film deposition, we have made micro-/nanoscale TFTC arrays in 3 × 3, 3 × 6, 5 × 5, 8 × 8, and 10 × 10 matrices from an area of 1 × 2 cm to an area of 5 × 5 μm. As a illustration, Figure 2 shows TFTC arrays with critical sizes of 20 μm and 500 nm, respectively. The TFTC array in Figure 2a dwells in an area of 1 × 1.2 mm, while another TFTC array in Figure 2b is around 5 × 5 μm, which is, to the best of our knowledge, the smallest TFTC array ever been made. They can provide precise local temperature mapping in highly scalable resolutions.

As to on-chip applications, a high surface density of TFTCs certainly increases the spatial resolution and accuracy in temperature measurement, but it also remarkably increases the number of pads and connections for the TFTC array, leading to complex interconnection. Therefore, the density of sensors in the array should be balanced between being enough to give required sensing resolution and being minimum to reduce the complexity of interconnection and space of pads.

We have found that matrices with relatively high densities were not necessary in integrated circuit temperature measurement since the 'hot spot' in a chip will provide temperature at least 20 times higher than the ambient temperature. Matrices of 3 × 3 or 3 × 6 TFTC array provided a temperature mapping good enough to help in judging where the hot spot was and how the thermal field time-dependently changed.

In addition, the density of TFTC array may have an influence on the real-time monitoring of local temperatures. Usually, one uses only one voltmeter to subsequently measure all the thermocouples in one array, with the help of a multiplexer. However, since a reliable reading process by a voltmeter needs a minimum time of 1 to 10 ms, if the total number of sensors in a TFTC array is too large, then one cycle of the measurements which ensures each individual sensor is measured once may take too long; thus, a real-time monitoring of the 2D temperature map may not be practical.

Results and discussion

Thermal 2D mapping Using multiplexing with high sampling rate in an array, one can easily obtain thermal readings of each TFTC in sequence. Given the heat that usually flows slowly and smoothly, an interpolation method can be applied to obtain the thermal mapping in different time windows. We have shown a multimedia movie to illustrate timeresolved temperature mapping by a TFTC array [15]. Moreover, more thermal information can be revealed by a simple built-in TFTC array for on-chip thermal analysis, which provided suitable array density and sampling rate. According to Fourier's law, if the temperature field T(x,y,t) can be obtained reliably, then a time-resolved heat flux vector field ⇀ q x; y; t ð Þ can be calculated directly from ⇀ q x; y; t ð Þ¼Àκ Á r ⇀ T x; y; t ð Þ. In chip failure analysis, heat flux data are usually more important for engineers to improve their design [23]. In our study, when a heating process commerced at the left side of the 3 × 6 TFTC array, a real-time heat flux mapping data were obtained, as shown in Figure 3.

Tracing the position of heat source

In on-chip applications, one cannot expect the hot spot to be always right on top of a TFTC. Unexpected failure in a working chip is always accompanied with unexpected hot spot induced. Tracing the possible locations of these unexpected hot spots is tricky for technicians. Inspired by a similar subject in signal processing, we propose to use a regular TFTC array to trace the heat.

In each contour line of a 2D map of local temperature field T(x,y,t), the temperature reads the same. From the heat flux field calculated from the gradient of T(x,y,t), we can even trace the heating source. By inversely tracing back the heat flow, one can find the source of the heat. Figure 4 shows two examples where a simple TFTC array of a 3 × 6 matrix is used to trace the heating source. The arrows in the figure are plotted inversely following the gradient of temperatures in the maps. In each figure, the red dot is the exact location of the inplane heater, while the grey-filled circle is the calculated location of heating source from the measured data. They actually match pretty well. Further work will be put on improving the precision of the source tracing.

Industrial on-chip applications

When putting the TFTC array in industrial applications, more possible problems need to be considered. One is that there are too many electrical pads induced with a TFTC array. A practical way to reduce the number of pads is to let a number of TFTCs share one common lead. By doing so, the pads and connections of TFTC array will shrink to nearly 50 % of the previous number. As the Cr-Ni thermocouple gives a relatively high thermopower, a common lead strategy can be adopted in designing without apparent error induced. Figure 5 shows an optical photograph of an 8 × 8 TFTC array that has the common lead configuration.

Another potential problem is that the temperature rises in the cold ends of TFTCs. In a TFTC built-in IC chip, because of the excellent thermal conductivity of silicon substrate when the IC circuit has been run for a long time, joule heat generated from the running current may heat up the entire chip, causing a remarkable rise of temperature at the cold ends of the TFTCs, thus causing a huge error in temperature readings. It seems that in this case, on-chip sensors of diodes or transistors can provide better temperature reading [24]. However, there are at least four defects which limit the development of these methods and why many endeavors were made in developing new ways of temperature sensing in IC chips. Firstly, such methods all require active parts like electrical sources, which bring additional consumption and self-induced heat. Secondly, diode, transistors, and thermistor sensors often exhibit nonlinear temperature characteristics in operating temperature range, and their property may vary sensitively to the fabrication process, so calibrations will be often adopted to test the temperature characteristic. Offset was also usually programmed into the sensors to give additional compensation. Thirdly, the diode sensors cannot be placed just in the hottest area of the chip because of routing and I/O limitations [25]. In chips with elements of high density like the Intel W CoreTM Duo processor, the hot spots tend to vary from place to place according to different loaded watt power. Imprecision from 2°C to 10°C caused by non-linearity and hot spot drifting was not strange by adopting diode temperature sensors [25].

In contrast, although the inherent defects of thermocouple-based sensor can just measure the temperature differences spanned on the device, they have all the merits of having no active parts, no electrical sources, being simple and cheap, having linear responses, and being repeatable and quick enough for time-resolved profile. Possible solutions to minimize the impact of temperature of cold end were addressed as follows:

It is true that the difficulty of local temperature mapping by TFTC array increases as the chip area is scaling down, especially for very small silicon-based chips, e.g., 5 × 5 mm. It will not be easy to carry out on-chip thermal management based on the TFTC array. However, one of the properties of TFTCs is that their property will not be affected by the device routing, and the output signal of TFTCs is only contingent with temperature differences between the hot ends and the cold ends. Thus, we can arrange a common cold end for all the TFTCs. As they are sharing one cold end, we can still map the relative temperature differences and locate the hot spot. In most situations, IC chips which need thermal management will not be as small as 5 × 5 mm, and the hot spots are usually distributed locally in only parts of the working components of high density [25], so the distance between the junction area and the cold end can easily exceed 1 cm, and arranging the cold end on the fringe of the silicon die will not provide significant measurement error. A cooling base or cooling fan will soon dissipate the heat at the marginal area of the chip. We have produced micro-or nano-TFTC arrays on silicon substrates from 1 × 1 cm to 4 inch in diameter, with pads on the wafer edges. The TFTC array still functioned well by simply referring the temperature of the pads as room temperature.

Conclusions

We have demonstrated micro-and nanoscale TFTC arrays as a powerful built-in thermal mapping tool. Figure 5 Optical photograph of a TFTC array with a common lead configuration. The array has 64 sensors arranged in an 8 × 8 square matrix, designed with a common lead configuration. The size of the array is 700 × 700 μm. Note that in the array, eight sensors in one series share one common lead, and all 64 sensors share one common bus line. Figure 4 Inverse tracing of the hot spot using a set of TFTC array. (a, b) Two cases that show the capability of tracing the heating source from 2D maps of local temperatures. By proper calculations, one can figure out the temperature fields and the flow of the heat that transfer throughout the substrate surface. The arrows in the figure are plotted inversely following the gradient of temperatures in the maps. In each figure, the red dot is the exact location of the in-plane heater, while the grey-filled circle is the calculated location of heating source from the measured data.

Using multiplexing technique, time-resolved temperature mapping can be easily drawn from TFTC array readings. Moreover, we have shown that TFTC array can also map real-time heat flux in plane, and the 2D mapping results can be used to precisely trace the heating source located in the surface.

Bearing in mind that the TFTC array can be used for on-chip solutions in the future, we discussed several remaining issues for its industrialization, i.e., choices of materials, density of sensor, sampling rate, common-lead strategy, and cold end temperature shift and solutions. We have demonstrated that a configuration of common lead can substantially reduce the number of pads by 50%.

We conclude that a variety of configuration of TFTC arrays is the most promising candidate as built-in sensors in 2D mapping of local temperature for solid devices such as IC chips because they are highly scalable from macro-to nanoscale, providing the potential of extremely high resolution and because they have a simple configuration, passive working mode, time-resolvable capability for real-time monitoring, and the capability for versatile applications.

Figure 2
2SEM micrograph of micro-/nanoscale TFTC array. (a) A TFTC array with 24 TFTCs in an area of around 1 × 1 mm. (b) A 3 × 3 TFTC array in an area of 5 × 5 μm, with a critical size of 500 nm.

Figure 3
3Time-resolved temperature and heat flux mapping data with slowly heated heat source located left side. The red text indicates the temperature rise in the isothermal lines. Along with the slow heating, the heat flux moved to indicate the direction of the heat source from the 10 s.
http://www.nanoscalereslett.com/content/7/1/484
AcknowledgmentsThis work was financially supported by NSFC (grant no. 11074010) and MOST of China (grant 2011CB933002).Competing interestsThe authors declare that they have no competing interests.Authors' contributions HXL carried out most of the experiments on sample preparation and dynamic thermal mapping. WQS designed some sample patterns and contributed valuable discussions. AX and TWS conducted preparation of some samples with e-beam lithography and helped in data analysis. QC contributed on important experimental resources. SYX conceived the study and coordinated experiments. All authors read and approved the final manuscript.
Dynamic surface temperature measurements in ICs. J Altet, W Claeys, S Dilhaire, A Rubio, Proc IEEE. 941519Altet J, Claeys W, Dilhaire S, Rubio A: Dynamic surface temperature measurements in ICs. Proc IEEE 2006, 94:1519.

Scanning thermal profiler. C Williams, H Wickramasinghe, Appl Phys Lett. 491587Williams C, Wickramasinghe H: Scanning thermal profiler. Appl Phys Lett 1986, 49:1587.

A luminescent molecular thermometer for long-term absolute temperature measurements at the nanoscale. C Brites, P Lima, N Silva, A Millán, V Amaral, F Palacio, L Carlos, C Brites, Adv Mater. 224499Brites C, Lima P, Silva N, Millán A, Amaral V, Palacio F, Carlos L, Brites C: A luminescent molecular thermometer for long-term absolute temperature measurements at the nanoscale. Adv Mater 2010, 22:4499.

Hydrophilic fluorescent nanogel thermometer for intracellular thermometry. C Gota, K Okabe, T Funatsu, Y Harada, S Uchiyama, J Am Chem Soc. 1312766Gota C, Okabe K, Funatsu T, Harada Y, Uchiyama S: Hydrophilic fluorescent nanogel thermometer for intracellular thermometry. J Am Chem Soc 2009, 131:2766.

Thermal analysis of integrated-circuit chips using thermographic imaging techniques. D H Lee, IEEE Trans Instrum Meas. 43824Lee DH: Thermal analysis of integrated-circuit chips using thermographic imaging techniques. IEEE Trans Instrum Meas 1994, 43:824.

Thermal conductivity of individual silicon nanowires. D Y Li, Y Y Wu, P Kim, L Shi, P D Yang, A Majumdar, Appl Phys Lett. 832934Li DY, Wu YY, Kim P, Shi L, Yang PD, Majumdar A: Thermal conductivity of individual silicon nanowires. Appl Phys Lett 2003, 83:2934.

The characteristics of Seebeck coefficient in silicon nanowires manufactured by CMOS compatible process. M Jang, Y Park, M Jun, Y Hyun, S Choi, T Zyung, Nanoscale Res Lett. 51654Jang M, Park Y, Jun M, Hyun Y, Choi S, Zyung T: The characteristics of Seebeck coefficient in silicon nanowires manufactured by CMOS compatible process. Nanoscale Res Lett 2010, 5:1654.

Transient temperature measurements of resist heating using nanothermocouples. D C Chu, W Wong, K Goodson, R Pease, J Vac Sci Technol B. 212985Chu DC, Wong W, Goodson K, Pease R: Transient temperature measurements of resist heating using nanothermocouples. J Vac Sci Technol B 2003, 21:2985.

Thermopile antennas for detection of millimeter waves. B Szentpáli, P Basa, P Fürjes, G Battistig, I Bársony, G Károlyi, T Berceli, V Rymanov, A Stöhr, Appl Phys Lett. 96133507Szentpáli B, Basa P, Fürjes P, Battistig G, Bársony I, Károlyi G, Berceli T, Rymanov V, Stöhr A: Thermopile antennas for detection of millimeter waves. Appl Phys Lett 2010, 96:133507.

Thermoelectric effect in very thin film Pt/Au thermocouples. M Salvadori, A Vaz, F Teixeira, M Cattani, I Brown, Appl Phys Lett. 88133106Salvadori M, Vaz A, Teixeira F, Cattani M, Brown I: Thermoelectric effect in very thin film Pt/Au thermocouples. Appl Phys Lett 2006, 88:133106.

Printed thick-film thermocouple sensors. S Duby, B Ramsey, D Harrison, Electron Lett. 41312Duby S, Ramsey B, Harrison D: Printed thick-film thermocouple sensors. Electron Lett 2005, 41:312.

Micro-temperature sensor array with thin-film thermocouples. J Park, M Taya, Electron Lett. 40599Park J, Taya M: Micro-temperature sensor array with thin-film thermocouples. Electron Lett 2004, 40:599.

J Y Long, A Klock, C L Zhou, S Memik, M Grayson, J Altet, B Courtois, M Rencz, A Rubio, Barcelona, Proc 16th THERMINIC. 16th International Workshop on Thermal Investigations of ICs and Systems. 16th THERMINIC. 16th International Workshop on Thermal Investigations of ICs and SystemsEDA PublishingIOTA: towards an integrated on-chip thermocouple arrayLong JY, Klock A, Zhou CL, Memik S, Grayson M: Proc 16th THERMINIC. 16th International Workshop on Thermal Investigations of ICs and Systems, September 2010. In IOTA: towards an integrated on-chip thermocouple array. Edited by Altet J, Courtois B, Rencz M, Rubio A. Barcelona: EDA Publishing; 2010.

Thermal sensing with lithographically patterned bimetallic thin-film thermocouples. A Varrenti, C L Zhou, A Klock, S Chyung, J Y Long, S Memik, M Grayson, IEEE Electron Dev Lett. 32818Varrenti A, Zhou CL, Klock A, Chyung S, Long JY, Memik S, Grayson M: Thermal sensing with lithographically patterned bimetallic thin-film thermocouples. IEEE Electron Dev Lett 2011, 32:818.

Thin-film thermocouple array for timeresolved local temperature mapping. H X Liu, W Q Sun, Q Chen, S Y Xu, IEEE Electron Dev Lett. 321606Liu HX, Sun WQ, Chen Q, Xu SY: Thin-film thermocouple array for time- resolved local temperature mapping. IEEE Electron Dev Lett 2011, 32:1606.

An extremely simple thermocouple made of a single layer of metal. H X Liu, W Q Sun, S Y Xu, Adv Mater. 243275Liu HX, Sun WQ, Xu SY: An extremely simple thermocouple made of a single layer of metal. Adv Mater 2012, 24:3275.

Thermal conductivity, electrical resistivity, and Seebeck coefficient of Silicon from 100 to 1300 K. W Fulkerson, J Moore, R Williams, R Graves, D Mcelroy, Phys Rev. 167765Fulkerson W, Moore J, Williams R, Graves R, McElroy D: Thermal conductivity, electrical resistivity, and Seebeck coefficient of Silicon from 100 to 1300 K. Phys Rev 1968, 167:765.

Miniaturized thermoelectric generators based on poly-Si and poly-SiGe surface micromachining. M Strasser, R Aigner, M Franosch, G Wachutka, Sens Actuator A. 535PhysStrasser M, Aigner R, Franosch M, Wachutka G: Miniaturized thermoelectric generators based on poly-Si and poly-SiGe surface micromachining. Sens Actuator A, Phys 2002, 535:97-98.

A batch-fabricated silicon thermopile infrared detector. G Lahiji, K Wise, IEEE Tran Electron Dev. 2914Lahiji G, Wise K: A batch-fabricated silicon thermopile infrared detector. IEEE Tran Electron Dev 1982, 29:14.

Thermoelectric infrared sensors by CMOS technology. R Lenggenhager, H Baltes, J Peer, M Forster, IEEE Electron Dev Lett. 13454Lenggenhager R, Baltes H, Peer J, Forster M: Thermoelectric infrared sensors by CMOS technology. IEEE Electron Dev Lett 1992, 13:454.

Micromachined thermally based CMOS microsensors. H Baltes, O Paul, O Brand, Proc IEEE. 861660Baltes H, Paul O, Brand O: Micromachined thermally based CMOS microsensors. Proc IEEE 1998, 86:1660.

Thermal sensors based on the Seebeck effect. A Herwaarden, P Sarro, Sens Actuator. 10321Herwaarden A, Sarro P: Thermal sensors based on the Seebeck effect. Sens Actuator. 1986, 10:321.

Heat-flux sensor to support transient thermal characterisation of IC packages. M Rencz, E Kollár, V Székely, Sens Actuator A. 116284PhysRencz M, Kollár E, Székely V: Heat-flux sensor to support transient thermal characterisation of IC packages. Sens Actuator A, Phys 2004, 116:284.

Diode temperature sensor array for measuring micro-scale surface temperatures with high resolution. I Han, S Kim, Sens Actuator A. 14152PhysHan I, Kim S: Diode temperature sensor array for measuring micro-scale surface temperatures with high resolution. Sens Actuator A, Phys 2008, 141:52.

E Rotem, J Hermerding, C Aviad, C Harel, B Courtois, M Rencz, C Lasance, V Szekely, Côte D'azur, 10.1186/1556-276X-7-484Proc 12th THERMINIC. 12th International Workshop on Thermal Investigations of ICs and Systems. 12th THERMINIC. 12th International Workshop on Thermal Investigations of ICs and SystemsEDA PublishingTemperature measurement in the Intel W CoreTM Duo processorRotem E, Hermerding J, Aviad C, Harel C: Proc 12th THERMINIC. 12th International Workshop on Thermal Investigations of ICs and Systems, September 2006. In Temperature measurement in the Intel W CoreTM Duo processor. Edited by Courtois B, Rencz M, Lasance C, Szekely V. Côte d'Azur: EDA Publishing; 2006. doi:10.1186/1556-276X-7-484

Towards on-chip time-resolved thermal mapping with micro-/nanosensor arrays. Liu, Nanoscale Research Letters. 484Cite this article asCite this article as: Liu et al.: Towards on-chip time-resolved thermal mapping with micro-/nanosensor arrays. Nanoscale Research Letters 2012 7:484.


Darwin's legacy in South African evolutionary biology

S D Johnson firstname.lastname@example.com
School of Biological and Conservation Sciences
University of KwaZulu-Natal
Private Bag X013209Scottsville, PietermaritzburgSouth Africa

Darwin's legacy in South African evolutionary biology
35E6F86A99830E4F995EA928916B7566Received 27 August. Accepted 2 November 2009.bibliometricsbiodiversity hotspotspeciationresearch trendsSouth Africaspecies concepts
Darwin's correspondents in South AfricaTowards the end of its famous voyage (1831-1836), the Beagle docked in Cape Town from 31 May to 18 June 1836.12,13arwin used this opportunity to meet local scientists, such as the astronomers John Herschel and Thomas Maclear, and to explore the adjacent coastal plain and mountains. 12Seemingly unimpressed, and apparently oblivious to the great botanical richness of the region, he commented that there 'was very little of interest' to be seen on these excursions.13Darwin did not travel abroad after returning to England and, in later years, seldom even attended scientific meetings in London.He consequently relied heavily on written correspondence with fellow naturalists around the world in order to obtain scientific information.Settler naturalists in South Africa were inspired by Darwin's books and papers, and several corresponded regularly with him.Of interest here is that many publications by these settler naturalists in the Journal of the Linnean Society were personally facilitated by Darwin.One of Darwin's most valued correspondents in South Africa was J.P. Mansell Weale, a naturalist who farmed in the eastern Cape region between 1860 and 1878.Weale shared Darwin's interest in the pollination mechanisms of orchids and other plants, and Darwin personally communicated several of Weale's papers for publication in the Journal of the Linnean Society.In 1871, Weale published a seminal paper on protective mimicry in the journal Nature, which was based on his field observations in South Africa.14uring the research leading up to the publication of The Expression of the Emotions in Man and Animals in 1871, Darwin distributed a questionnaire with a view to learning more about the cultural traditions of the 'native' inhabitants of the colonies.In particular, he was interested in testing his hypothesis that universality of expression of emotions reflects common descent.Darwin was interested in the expression of emotions in the Xhosa people of the eastern Cape, and enlisted the help of Weale to distribute copies of his questionnaire.15An interesting

Introduction

The publication of Darwin's Origin of Species in 1859 1 marked one of the great revolutions in science.Darwin's central idea, that species diverged through natural selection and are thus related by a branching pattern of common descent, provided a new materialistic explanation for the diversity of the natural world.

How did evolutionary biology develop in South Africa over the subsequent 150 years, and what were the milestones along the way?What are its current strengths and roles in a modern democratic South Africa?To address these questions I review the South African literature on evolutionary biology, first as an historical narrative, and second with respect to noteworthy research themes.I also consider the extent to which sociological misinterpretation of Darwin's ideas had an influence on the development of racist ideology in South Africa.Finally, I present the results of a bibliographic analysis of publication trends in evolutionary biology for South Africa, relative to other countries which cover the range from developing to developed economies and low to high biodiversity.

The biological sciences, together with geological and medical sciences, have historically been relatively strong components of the research system in South Africa. 2,3In the case of biological and geological sciences, the most likely explanation for this is that these benefit particularly from the rich natural resources of the region. 4Evolutionary biology, in particular, has benefited from the extraordinary diversity of plant, mammal, bird and invertebrate species, as well as the key fossil hominid discoveries in the region.

][7][8][9][10][11] Pockets of South African excellence can be identified in several subdisciplines of evolutionary biology, including hominid palaeontology, systematics, species concepts, speciation research, the study of adaptation, and coevolution.Before considering the specific contributions that have been made to these subdisciplines, I sketch the historical development of evolutionary biology in South Africa from the time of Darwin.In the two decades after publication of the Origin of Species, Charles Darwin facilitated the publication of numerous scientific papers by settler naturalists in South Africa.This helped to establish the strong tradition of natural history which has characterised evolutionary research in South African museums, herbaria and universities.Significant developments in the early 20th century included the hominid fossil discoveries of Raymond Dart, Robert Broom, and others, but there was otherwise very little South African involvement in the evolutionary synthesis of the 1930s and 1940s.Evolutionary biology developed into a distinct discipline in South Africa during the 1970s and 1980s when it was dominated by mammalian palaeontology and a vigorous debate around species concepts.In the post-apartheid era, the main focus of evolutionary biology has been the construction of phylogenies for African plants and animals using molecular data, and the use of these phylogenies to answer questions about taxonomic classification and trait evolution.South African biologists have also recently contributed important evidence for some of Darwin's ideas about plant-animal coevolution, sexual selection, and the role of natural selection in speciation.A bibliographic analysis shows that South African authors produce 2-3% of the world's publications in the field of evolutionary biology, which is much higher than the value of about 0.5% for publications in all sciences.With its extraordinary biodiversity and well-developed research infrastructure, South Africa is an ideal laboratory from which to advance evolutionary research.

historical aside is that Darwin, who had expected his questionnaires to be completed by settlers, was somewhat taken aback to receive one with answers written in English by Christian Ngqika, a Xhosa constable working in the frontier town of Bedford.

Darwin also corresponded with Mary Elizabeth Barber, an amateur naturalist based in Grahamstown.Barber was the first woman to be admitted as a member of the South African Philosophical Society (later to become the Royal Society of South Africa) and was an accomplished painter and plant collector.Like Weale, Barber was interested in the pollination mechanisms of plants and published several papers on the topic with the assistance of Darwin. 16arber readily incorporated Darwin's concept of natural selection into her own settler ideology of race.In several of her letters, she expressed views that made it clear that she considered the dominant position of Europeans in the colony to be a consequence of a natural biological hierarchy.In a thoughtful paper, Robert Shanafeldt 15 argues that Darwin should have foreseen the potential for his ideas to reinforce and justify the existing attitudes of the settlers.He describes Darwin's own views as 'tepid humanism', meaning that he neither condoned nor actively opposed these developments.

As amateur naturalists, Weale and Barber did not leave any institutional legacy of evolutionary biology in South Africa.By contrast, Roland Trimen, another of Darwin's correspondents, played an important role in the development of the South African Museum as its first director.Trimen was initially the private secretary to the then Colonial Secretary Sir Henry Barkly (1815-1898), who was also an amateur botanist and instrumental in encouraging the development of science at the Cape. 17arwin facilitated the publication of Trimen's first scientific paper, which was on the functional morphology of the orchid Disa grandiflora (now Disa uniflora), 18 but Trimen is best known for his work on the butterflies of South Africa, including a book he coauthored with James Henry Bowker (Mary Barber 's brother). 19Trimen, like Weale and Barber, was very interested in mimicry. 17In a pioneering paper, Trimen, with help from Barber and Weale, identified various mimetic female forms of the butterfly Papilio dardanus. 20atural history declined towards the end of the 19th century both in South Africa and abroad, although it was kept alive by systematists working in museums.Several universities were established in South Africa around the turn of the century, 21 but it would be some time before evolutionary research would be an integral part of their curricula.

The early 20th century

The most significant South African contribution to evolutionary biology, and arguably the most important contribution of the country to science generally, resulted from the discovery in 1924 of a well-preserved skull of a juvenile hominid in a limeworks quarry at Taung, near Kimberley.The significance of this specimen as a potential 'missing link' between apes and modern humans was recognised by Raymond Dart, the newly appointed head of the Department of Anatomy at the University of the Witwatersrand, who named the 'ape-man' Australopithecus africanus. 22Dart inferred from the skull morphology that A. africanus was bipedal, and (with considerable verve given that he was just 32 and outside the scientific mainstream) wrote that the discovery could vindicate the 'Darwinian claim that Africa would prove to be the cradle of mankind'.This claim was met with considerable skepticism by the palaeontological community, first because Darwin's prediction about the emergence of man in Africa in his book, The Descent of Man, had been overlooked in favour of the idea that humans evolved in Asia, and second because it had been assumed that bipedalism evolved only after the evolution of a large cranium (which the Taung child did not possess).Robert Broom, a physician and palaeontologist, who had described many new fossil mammal-like reptiles in the early part of his career, became Dart's major ally in South Africa.Broom discovered several adult specimens of A. africanus, as well as a new robust hominid Paranthropus robustus from the Kromdraai diggings in the 1930s and 1940s. 23hese and other discoveries eventually vindicated the Darwin-Dart hypothesis about the African origin of humankind.

Recent historical research has uncovered a number of important links between biological science and the development of racist ideology in early 20th century South Africa. 24Harold B. Fantham, the first Professor of Zoology at the University of the Witwatersrand from 1917-1932, was an outspoken proponent of eugenics and, in a series of articles published in this journal, argued for the need for the state to take measures to maintain 'race purity'. 24Fantham also had an influence on the geneticist Gerrit Eloff, head of the Department of Genetics and Breeding Studies at the University of the Orange Free State and an admirer of the German Nazi movement, who developed pseudobiological arguments for the adaptiveness of Afrikaners to Africa and thus the supposed imperative to maintain the purity of their gene pool. 24an Smuts, prime minister from 1919 to 1924 and again from 1939 to 1948, was an amateur botanist with a strong interest in evolutionary theory, biogeography, and human origins.While at Stellenbosch University, Smuts had studied taxonomy under Rudolf Marloth, the author of Flora of South Africa, whom he later accompanied on many plant-collecting expeditions.Smuts served as the president of the South African Association for the Advancement of Science (S2A3) in 1925, and even intervened personally to secure a position for Robert Broom at the Transvaal Museum.The two men had a close relationship and shared rather unorthodox teleological views on evolution.Saul Dubow has termed Smuts a 'scientific nationalist'. 21However, Smuts' 'holism' is scarcely compatible with Darwin's theory that selection acts on individuals, although it does share with Social Darwinism the dangerous premise that biological laws should be the inspiration for human society.

Jeffrey Lever 25 has described Social Darwinism as an 'intellectual pathogen' that was imported from Europe and used to reinforce the pre-existing folk ideologies of racial superiority among white South Africans.However, with some notable exceptions, 21,24 there have been few studies of the actual extent of its influence on the development of policies of racial segregation.By and large, Christian Nationalists tended to justify racial segregation on the basis of a divine mandate, rather than the pseudoscience of Social Darwinism.Darwin's theory, its main buttress, was rejected on religious grounds by nationalists that took power in 1948, and it was not until after the first democratic elections in 1994 that evolution was even permitted to be taught again in schools. 25outh African evolutionary biologists had very little to do with the evolutionary synthesis of the 1930s and 1940s, and the second half of the 20th century, until 1990, was characterised by the academic isolation of the apartheid era.

The late 20th century to the present day

The groundbreaking work by Dart and Broom helped to establish palaeontology as one of the strongest branches of science in South Africa during the second half of the 20th century, with a steady stream of new discoveries, and the development of top-class facilities, such as the Bernard Price Institute for palaeontological research at the University of the Witwatersrand.Leading palaeontologists of this period included Philip Tobias, Bob Brain and Elisabeth Vrba, while groundbreaking work on the genetics of modern humans was conducted by Trefor Jenkins and Himla Soodyall.

The University of the Witwatersrand (Wits) was indisputably the leading centre for evolutionary biology in South Africa during this period.The zoologist Hugh Paterson, who was based at Wits, developed the 'recognition' species concept in the 1970s, which strongly influenced a generation of South African biologists.Paterson's influence is especially evident in the book Species and Speciation, edited by Elisabeth Vrba. 26This book contained contributions from a wide range of botanists, zoologists and palaeontologists who had participated in a symposium at the Transvaal Museum in 1982.The 1980s were also characterised by the emigration of many leading evolutionary biologists; this is evidenced in the change of addresses for fully one third of the authors in Species and Speciation between the time of the symposium and publication of the book in 1985.The published opening address by the then chairman of Anglo-American Michael O'Dowd was singled out in a review of the book by the leading American systematist Michael Donoghue for containing 'a form of biological determinism' that could be cited as justification for apartheid. 27Although these charges were perhaps unfair since O'Dowd had actually emphasised the distinction between biological and social evolution, they nevertheless highlight the considerable political of that decade.

The end of apartheid and the first democratic elections in 1994 brought an end to the formal and informal isolation of academia in South Africa.New collaborations with scientists in other countries were forged, and evolutionary biology was strengthened in many universities.This period of optimism also coincided with the new availability of the technique of automated DNAsequencing that gave biologists a source of vast amounts of new molecular data with which to construct phylogenies for plant and animal groups.And in 1999, Sterkfontein and other fossil hominid sites received recognition as the UNESCO 'Cradle of Humankind' World Heritage Site.

In this penultimate part of the review I explore specific themes which have been a focus of research efforts by South African evolutionary biologists in both the past and the present centuries.

Species concepts and speciation

Darwin considered species as arbitrarily defined entities resulting from adaptive divergence. 1 He explained the discontinuities between species as the result of extinctions rather than breeding barriers. 28His view that species did not differ in any profound sense from intraspecific levels of the taxonomic hierarchy was probably a deliberate attempt to counter the prevailing creationist notion that species have a special status in nature.This led to later claims that Darwin failed to solve the 'species problem' and that the title of his book On the Origin of Species was misleading. 29However, Darwin's uniformitarian view of species has enjoyed considerable support, particularly from botanists, 30 and is being increasingly advocated by zoologists who find the idea consistent with both morphological and molecular evidence. 31n contrast to Darwin, Dobzhansky 32 and Mayr 33 considered species to have a distinct property: reproductive isolation from other species.There are now a plethora of different species concepts, but their biological species concept (BSC) is by far the most widely accepted, especially among zoologists. 29The BSC was attacked by the South African biologist Hugh Paterson in a series of articles, many published in this journal, during the 1970s and 1980s. 6,34In its place, Paterson proposed the 'recognition' concept of species which emphasised the reproductive cohesiveness of species arising from a 'specific mate recognition system' (SMRS).As a concept of species, it was rather similar to the 'cohesion' concept developed by Templeton, 35 and Carson's (1957) concept of the species as a 'field for gene recombination'. 36he recognition concept had a major influence on the development of evolutionary thought in South African universities and museums.

Paterson was particularly opposed to the idea that reproductive systems evolve through a process of reinforcement (selection for traits that limit hybridisation in a secondary contact zone). 6,37His dismissal of the latter possibility was based on the simple observations that most speciation is allopatric and that even if traits were selected through reinforcement in a secondary contact zone, such traits would not have fitness value outside the contact zone and therefore be unlikely to be fixed at the species level.However, Paterson has been justifiably criticised for over-emphasising the dependence of the BSC on reinforcement and then attacking this formulation of the BSC as a straw man. 38hile it is true that Dobzhansky, in particular, commonly invoked reinforcement to explain differences in reproductive characters, 32 Mayr tended to emphasise pleiotropy as the explanation for divergence in reproductive characters. 33ayr 's emphasis 33 on pleiotropy as the explanation for the building of reproductive isolating barriers in allopatry was plausible for some aspects, such as genetic incompatibility, but was an unsatisfactory explanation for divergence in the complex reproductive characters, e.g.genitalia, that are often used to diagnose species.By contrast, Paterson 6,39 emphasised the direct role of selection for traits that improve mating success as an explanation for divergence in reproductive systems.He, and others at the time, tended to emphasise the role of the physical environment in this process, 40 but sexual selection provides another, even more potent, force for allopatric divergence in reproductive systems.Mary West-Eberhard's classic review of the role of sexual selection in speciation 41 provided some of the missing pieces of the puzzle of why adaptive radiations so often involve reproductive traits, although she was seemingly unaware of Paterson's work at that stage.Her apparently independent conclusion that sexual selection could drive the divergence of systems of 'species recognition' in allopatric animal populations was uncannily close to Paterson's concept of speciation.

Paterson struggled to develop a useful definition of an SMRS in plants, and specifically excluded asexual organisms from his concept, and thus, like Mayr, did not succeed in developing a universal genetic species concept.With the hindsight of history, Paterson made a valuable contribution in emphasising the importance of allopatric divergence of reproductive systems under selection for increased mating success, and inspired South African biologists (and the few elsewhere who read his work) to think more deeply about the process of speciation.However, he did not provide a species definition that was much more useful than the BSC, and this may be because he accepted the prevailing dogma that species are special units of organisation in nature, as opposed to a convenient label for profoundly divergent forms, as advocated by Darwin and several contemporary evolutionary biologists. 30,31he extraordinary biodiversity of South Africa has been a major inspiration for evolutionary biologists.Why are there so many species, and why are there particular concentrations of species in some regions?Elisabeth Vrba 8 made an important early contribution by emphasising the role of natural selection in changing environments at a time when most models of speciation involved non-adaptive processes, such as drift.In recent years there has been a special focus on speciation of plant species in the Cape floristic region. 42,43Dating using calibrated molecular clocks suggests that some groups have radiated very rapidly 44,45 while others have been present in this region for at least 30 million years. 43Hypotheses for high rates of diversification have ranged from habitat heterogeneity combined with shortdistance gene flow, 46 to the role of fire in enforcing isolation between populations, 47 to selection imposed by a geographical mosaic of pollinator availability. 30All of these models have at least some empirical support [48][49][50][51][52] and current consensus favours a plurality of explanations, including the possibility of low extinction rates which allows species to accumulate in a particular region. 53,54aptation: from functional morphology to the comparative method

Studies of functional morphology were the main focus of evolutionary studies in the Darwin era.This was premised on the idea that if a trait could be shown to have a function it was likely to have evolved through natural selection.In the 1970s, Stephen Jay Gould, in collaboration with Richard Lewontin and the South African palaeontologist Elisabeth Vrba, published two important caveats to this approach, first pointing out that many traits are, in the historical sense, 'exaptations' whose current utility differs from their evolved function, 55 and that other traits are simply byproducts of the Bauplan (blueprint) of the organism, rather than direct products of selection. 56volutionary ecologists in South Africa have long sought to understand how the plants in the wide diversity of biomes in the region have adapted to their local physical environments. 48,52,57otable contributions include studies of the significance of resprouting, 58 resource allocation in grasses adapted to different soils, 52 and the adaptations of plants to fire. 57Fire is a major shaper of ecosystems in South Africa and models show that in its absence large areas of the subcontinent would be covered in forest. 59ne of Darwin's favourite research themes was the floral adaptations of plants to their pollinators. 60South African biologists have provided some of the clearest examples of floral adaptation, including striking examples of Batesian floral mimicry (non-rewarding flowers that imitate the advertising signals of rewarding flowers). 61he first conceptualisation of coevolution was made in Darwin's book on orchid pollination 62 in which he speculated that the very long spurs of the Malagasy orchid Angraecum sesquipedale evolved under selection for efficient pollination by an as-yet-unknown giant hawkmoth with an exceedingly long proboscis which, in turn, evolved under selection to obtain the 'last drop' of nectar at the tip of the orchid's spur.4][65] For example, in a mutualism between oil-producing flowers and oil-collecting bees in the Drakensberg mountains, there is striking population-level covariation between the flower depth in a guild of flowers and the length of the highly elongated front legs of one of the bee species (they use their front legs to scrape oil from the flowers). 63imilarly, long-proboscid flies and their nectar host plants show geographically structured patterns of covariation that are consistent with coevolution. 64,65ecause species tend to share trait values through common descent, any statistical analysis that assumes independence among species trait values may be invalid. 668][69] In one study, 70 the comparative method was used to establish the significance for cross-pollination of the time taken for orchid pollinaria to reconfigure after withdrawal from flowers (an issue that particularly intrigued Darwin).In another, 68 it was used to identify large variations in patterns of metabolic rate in mammals, corresponding to the major zoogeographical zones of the world.These regional differences appear to reflect adaptation to climate, especially ambient temperatures and rainfall unpredictability, 69 and thus challenge the prevailing paradigm of a nonadaptive mechanistic determination of mammalian metabolism.

Studies on insects also point to metabolic adaptation to climate. 71arwin contributed many important secondary ideas to the science of evolutionary biology, including sexual selection and coevolution.Avian biologists have been at the forefront of sexual selection studies in South Africa.Some of the most notable contributions have included the demonstration that the multiple ornamentation of a red collar and long tail in male widow birds represent the result of selection through male-male competition and female choice, respectively, with a trade-off evident in investment in these two signal functions. 72,73Avian biologists have also provided convincing evidence for egg mimicry by parasitic birds. 74South African researchers Jenny Jarvis and Nigel Bennett have played a leading role in understanding the evolution of eusociality in mammals. 75,76

Systematics

Systematics, the study of evolutionary relationships among organisms and their classification, is a scientific field which benefits directly from the rich biodiversity of South Africa.Systematics has always depended on collections and has thus been a key aspect of research in the major South African museums and herbaria from the time of their formation in the late 19th century.

Botanical systematics was a core function of the South African National Botanical Institute, which in 2004 became the South African National Biodiversity Institute with an expanded mandate to cover animal diversity.Other important developments were the formation of the Southern African Society for Systematic Biology in 1999 and the South African Biosystematics Initiative, a National Research Foundation (NRF)-managed funding initiative of the Department of Science and Technology (DST), which supports research in the general field of systematics.The past two decades have seen a considerable strengthening of phylogenetics, the specific component of systematics that deals with evolutionary relationships, and a weakening of capacity in traditional taxonomy, especially for species-rich groups like insects.

The phylogenetics of the Cape flora has received close scrutiny over the past two decades, 42,43 with notable contributions including a phylogeny based on exemplars of most of the genera in the flora, 77 evidence for rapid radiations in some groups, 44 and the use of dated phylogenies to answer questions about the age of the Cape and Namaqualand floras. 43,78An important spin-off from these phylogenetic studies has been the gaining of deeper insights into biogeographic affinities of floras. 79,80outh Africa does not have a unique zoogeographical region equivalent to the Cape flora, but has a notable diversity of mammals, birds and some insect groups.Phylogenetic studies of mammals have focused on the relationships within the Afrotheria, a largely African clade that includes elephants and aardvarks, 81 and the relationships of this group to the other placental Review Articles mammals. 82Studies of the population genetics and phylogeny of fishes have been valuable in understanding the evolution of river drainage systems in South Africa. 83

Publication trends

To assess the position of evolutionary biology relative to other fields in South Africa and to determine how the global contribution of this field in South Africa compares with four other countries varying in development status and biodiversity, I conducted a bibliographic analysis using the Thomson Reuters ISI Web of Science ® .Countries that were compared to South Africa were New Zealand, a southern hemisphere country whose total research output is almost identical to that of South Africa and which, like South Africa, has a natural advantage in evolutionary biology on account of its highly endemic fauna and flora and isolated biogeographical position; Brazil, a developing country with a megadiverse fauna and flora; China, which has one of the world's fastest growing economies and research environments; and Switzerland, a wealthy developed country with relatively low levels of biodiversity.

I first calculated the year-by-year (1990-2008) trends in the percentage of papers in the ISI Web of Science ® database that are contributed by authors in the five countries.This was done to assess the performance of the overall science system in these countries.I then did a year-by-year (1990-2008) search for the keywords 'species', 'speciation', 'phylogeny' and 'adaptation' within six of the major biological knowledge fields (plant sciences, zoology, entomology, evolutionary biology, biology and ecology) in the Science Citation Index.This was done for the five countries, as well as the entire database, to assess the performance of the countries relative to global output in the field of evolutionary biology.This analysis cannot provide an absolute measure of outputs because of the limitations of the keywords, but can provide relative measures among countries and the entire database.The analysis proved robust to removal or addition of search terms.For example, the keyword 'species' was included on the grounds that taxonomy is part of evolutionary biology, but the trends obtained with and without this keyword were almost identical.

South Africa contributes about 2-3% of world output in the field of evolutionary biology, a value which has declined slightly over the past two decades (Fig. 1a).Very similar percentages and trends were obtained for New Zealand and Switzerland (Fig. 1a).In contrast, China and Brazil have shown a steep rise in their 'market share' of world publications of evolutionary biology papers, from positions similar or below those of South Africa, New Zealand and Switzerland in the early 1990s to contributions of about 6% and 7% of the world's output in 2008, respectively (Fig. 1a).

The contributions of South Africa, New Zealand and Brazil to evolutionary biology are all about four-fold greater than their proportional contributions to all world science publications (Fig. 1), suggesting that they have particular strengths in evolutionary biology and this is likely related to their natural advantages in terms of biodiversity.For China and Switzerland, on the other hand, the strength of evolutionary biology is roughly equivalent to that of the other sciences (Fig. 1).

These analyses are admittedly crude and do not take the citation impact of publications into account. 3However, analysis of author affiliations of papers published in the leading journals in evolutionary biology over the past five years revealed a relatively healthy level of contributions from South Africa: Biological Journal of the Linnean Society (2.4%), Evolution (0.8%), Journal of Evolutionary Biology (1.1%), Proceedings of the Royal Society (London): Biological Sciences (2.1%), and Molecular Phylogenetics and Evolution (3.5%).This suggests that South African authors are making important conceptual advances in this field.

Conclusion

This review has identified evolutionary biology as a particularly strong field within the South African research system with a long tradition that can be traced back to Darwin.However the natural advantage that South Africa enjoys in this field has not yet been exploited to the full.Over time, it would be expected that countries with the richest biodiversity should make the most important contributions to evolutionary biology.Questions must be raised, therefore, about why other developing countries, such as Brazil, have managed to increase their share of world publications in this field over the past two decades, while South Africa has not (Fig. 1).One constraint on future growth is the legacy of years of willful neglect of evolutionary biology in the school curriculum, 25 combined with the persistence of poor schooling conditions for the majority of South Africans.These factors probably explain why ordinary citizens of South Africa fared the worst of those in any of the countries recently surveyed for understanding of Darwin's theory (British Council Press Release http://www.britishcouncil.org/darwinnow-survey-global.pdf).Equipping citizens with the means to comprehend the enormous relevance of evolutionary biology is essential, not only for the basic sciences, but also for applied disciplines that are impacted by evolutionary processes, such as medicine, 84 invasion biology, 85 and conservation biology. 86

406

Fig. 1 .
1
Fig. 1.The percentage of global publications in (a) evolutionary biology, and in (b) all sciences, contributed by authors based in South Africa, Brazil, China, Switzerland and New Zealand over the period 1990-2008.

South African Journal of Science 105, November/December 2009

On the Origin of Species by Means of Natural Selection or the Preservation of Favoured Races in the Struggle for Life. Darwin C , 1859John MurrayLondon

South African research in the context of Africa and globally. M Jeenah, A Pouris, S. Afr. J. Sci. 1042008

South Africa's research publication record: the last ten years. A Pouris, S. Afr. J. Sci. 992003

The scientific wealth of nations. R M May, Science. 2751997

Evolution, species and fossils -how does life evolve. E S Vrba, S. Afr. J. Sci. 761980

More evidence against speciation by reinforcement. H E H Paterson, S. Afr. J. Sci. 741978

Australopithecus africanusits phyletic position reconsidered. T D White, D C Johanson, W H Kimbel, S. Afr. J. Sci. 771981

Environment and evolution -alternative causes of the temporal distribution of evolutionary events. E S Vrba, S. Afr. J. Sci. 811985

Trophic differences between gracile and robust australopithecines -a scanning electron-microscope analysis of occlusal events. F E Grine, S. Afr. J. Sci. 771981

Perspective on speciation by reinforcement. H E H Paterson, S. Afr. J. Sci. 781982

The continuing search for the unknown and unknowable -a critique of contemporary ideas on speciation. H E H Paterson, S. Afr. J. Sci. 771981

Darwin as a plant scientist: a southern hemisphere perspective. S D Hopper, H Lambers, Trends Plant Sci. 142009

Charles Darwin's Beagle Diary. R D Keynes, 1988Cambridge University PressCambridge

Protective resemblances. J P M Weale, Nature. 31871

How Charles Darwin got emotional expression out of South Africa (and the people who helped him). R Shanafelt, Comp. Stud. Soc. Hist. 452003

On the structure and fertilization of Liparis bowkeri. M E Barber, J. Linn. Soc. 51869

Roland Trimen and the Merope harem. A Cohen, Notes Rec. Roy. Soc. 562002

On the fertilization of Disa grandiflora. R Trimen, J. Linn. Soc. 71864

R Trimen, J H Bowker, South-African Butterflies: A Monograph of the Extra-Tropical Species. LondonTrubner & Co1887

On some remarkable mimetic analogies among African butterflies. R Trimen, Trans. Linn. Soc. Lond. 261869

S Dubow, A Commonwealth of Knowledge: Science, Sensibility and White South Africa 1820-2000. OxfordOxford University Press2006

Australopithecus africanus: the man-ape of South Africa. R A Dart, Nature. 1151925

The South African fossil ape-man: the Australopithecinae. R A Broom, G W H Scheepers, Trans. Mus. Memoir. 21946

S Dubow, Scientific Racism in Modern South Africa. CambridgeCambridge University Press1995

Science, Evolution and Schooling in South Africa. J Lever, Africa Human Genome Initiative. 2002

Species and Speciation. Transvaal Museum. E S Vrba, Pretoria1985

South African perspectives on species: an evaluation of the recognition concept. M J Donoghue, Cladistics. 21987

Darwin's bridge between microevolution and macroevolution. D N Reznick, R E Ricklefs, Nature. 4572009

J A Coyne, H A Orr, Speciation. Sunderland, MASinauer Associates Inc2004

Pollinator-driven speciation in plants. S D Johnson, The Ecology and Evolution of Flowers. L D Harder, S C H Barrett, OxfordOxford University Press2006

Hybridization, ecological races and the nature of species: empirical evidence for the ease of speciation. J Mallet, Phil. Trans. Roy. Soc. Lond. B. 3632008

Genetics and the Origin of Species, 3 edn. T Dobzhansky, 1951Columbia University PressNew York

Animal Species and Evolution. E Mayr, 1963Belknap PressCambridge

The continuing search for the unknown and unknowable: a critique of contemporary ideas on speciation. H E H Paterson, S. Afr. J. Sci. 771981

The meaning of species and speciation. A R Templeton, Speciation and its Consequences. D Otte, J A Endler, Sunderland, MASinauer Associates1989

The species as a field for gene recombination. H L Carson, The Species Problem. E Mayr, Washington D.CAmerican Association for the Advancement of Science1957

Perspective on speciation by reinforcement. H E H Paterson, S. Afr. J. Sci. 781982

The recognition species concept: is it really an alternative. D Raubenheimer, T M Crowe, S. Afr. J. Sci. 831987

The recognition concept of species. H E H Paterson, In Trans. Mus. Monogr. E.S. Vrba41985Transvaal Museum

Environment and species. H E H Paterson, S. Afr. J. Sci. 821986

Sexual selection, social competition, and speciation. M West-Eberhard, Q. Rev. Biol. 581983

Understanding the origins and evolution of the world's biodiversity hotspots: The biota of the African 'Cape Floristic Region' as a case study preface. G A Verboom, L L Dreyer, V Savolainen, Mol. Phylogenet. Evol. 512009

Evolution of diversity: the Cape flora. H P Linder, Trends Plant Sci. 102005

Unmatched tempo of evolution in southern African semi-desert ice plants. C Klak, G Reeves, T Hedderson, Nature. 4272004

Rapid and recent origin of species richness in the Cape flora of South Africa. J E Richardson, F M Weitz, M F Fay, Q C B Cronk, H P Linder, G Reeves, M W Chase, Nature. 4122001

Gene flow, speciation and species diversity patterns in a species-rich area: the Cape flora. H P Linder, Trans. Mus. Monogr. Species and Speciation, ed. E.S. Vrba41985Transvaal Museum

Fire and its role in coexistence and speciation in Gondwanan shrublands. R M Cowling, S. Afr. J. Sci. 831987

Coexistence and differentiation of 'flowering stones': the role of local adaptation to soil microenvironment. A G Ellis, A E Weis, J. Ecol. 942006

Evolutionary radiation of "stone plants" in the genus Argyroderma (Aizoaceae): Unraveling the effects of landscape, habitat, and flowering. A G Ellis, A E Weis, B S Gaut, Evolution. 602006

Phylogeny and radiation of pollination systems in Disa (Orchidaceae). S D Johnson, H P Linder, K E Steiner, Am. J. Bot. 851998

Long-tongued fly pollination and evolution of floral spur length in the Disa draconis complex (Orchidaceae). S D Johnson, K E Steiner, Evolution. 511997

Testing the adaptive nature of radiation: growth form and life history divergence in the African grass genus Ehrharta (Poaceae: Ehrhartoideae). G A Verboom, H P Linder, W D Stock, Am. J. Bot. 912004

OCBIL theory: towards an integrated understanding of the evolution, ecology and conservation of biodiversity on old, climatically buffered, infertile landscapes. S D Hopper, Plant Soil. 3222009

Patterns of plant speciation in the Cape floristic region. T Van Der Niet, S D Johnson, Mol. Phylogenet. Evol. 512009

Exaptation -a missing term in the science of form. S J Gould, E S Vrba, Paleobiology. 81982

The spandrels of San-Marco and the Panglossian paradigm -a critique of the adaptationist program. S J Gould, R C Lewontin, Proc. Roy. Soc. Lond. B. 2051979

Fire as a global 'herbivore': the ecology and evolution of flammable ecosystems. W J Bond, J E Keeley, Trends Ecol. Evol. 2005

Ecology of sprouting in woody plants: the persistence niche. W J Bond, J J Midgley, Trends Ecol. Evol. 162001

The global distribution of ecosystems in a world without fire. W J Bond, F I Woodward, G F Midgley, New Phytol. 1652005

Darwin's beautiful contrivances: evolutionary and functional evidence for floral adaptation. L D Harder, S D Johnson, New Phytol. 1832009

Batesian mimicry in the non-rewarding orchid Disa pulchra, and its consequences for pollinator behaviour. S D Johnson, Biol. J. Linn. Soc. 712000

On the Various Contrivances by which British and Foreign Orchids are Fertilized by Insects, facsimile edn. C R Darwin, 1862John MurrayLondon

Pollinator adaptation to oil-secreting flowers -Redivivia and Diascia. K E Steiner, V B Whitehead, Evolution. 441990

The geographical mosaic of coevolution in a plant-pollinator mutualism. B Anderson, S D Johnson, Evolution. 622008

A Pauw, J Stofberg, R J Waterman, Flies and flowers in Darwin's race. 200963

Phylogenies and the comparative method. J Felsenstein, Am. Nat. 1251985

Adaptation and constraint in the evolution of the physiology and behavior of the namib desert tenebrionid beetle genus Onymacris. D Ward, M K Seely, Evolution. 501996

The zoogeography of mammalian basal metabolic rate. B G Lovegrove, Am. Nat. 1562000

The influence of climate on the basal metabolic rate of small mammals: a slow-fast metabolic continuum. B G Lovegrove, J. Comp. Physiol. B. 1732003

Doing the twist: a test of Darwin's cross-pollination hypothesis for pollination reconfiguration. C I Peter, S D Johnson, Biol. Lett. 22006

Metabolic cold adaptation in insects: a large-scale perspective. A Addo-Bediako, S L Chown, K J Gaston, Funct. Ecol. 162002

Multiple receivers, multiple ornaments, and a trade-off between agonistic and epigamic signaling in a widowbird. S Andersson, S R Pryke, J Ornborg, M J Lawes, M Andersson, Am. Nat. 1602002

Sexual selection of multiple handicaps in the red-collared widowbird: female choice of tail length but not carotenoid display. S R Pryke, S Andersson, M J Lawes, Evolution. 552001

Egg colour matching in an African cuckoo, as revealed by ultraviolet-visible reflectance spectrophotometry. M I Cherry, A T D Bennett, Proc. Roy. Soc. Lond. B. 2682001

Mammalian eusociality -a family affair. J U M Jarvis, M J O'riain, N C Bennett, P W Sherman, Trends Ecol. Evol. 91994

Ecological constraints drive social evolution in the African mole-rats. C G Faulkes, N C Bennett, M W Bruford, H P O'brien, G H Aguilar, J U M Jarvis, Proc. Roy. Soc. Lond. B. 2641997

Preserving the evolutionary potential of floras in biodiversity hotspots. F Forest, R Grenyer, M Rouget, T J Davies, R M Cowling, D P Faith, A Balmford, J C Manning, Ô Procheõ, M Van Der Bank, G Reeves, T A J Hedderson, V Savolainen, Nature. 4452007

Origin and diversification of the Greater Cape flora: Ancient species repository, hot-bed of recent radiation, or both? Mol. G A Verboom, J K Archibald, F T Bakker, D U Bellstedt, F Conrad, L L Dreyer, F Forest, C Galley, P Goldblatt, J F Henning, K Mummenhoff, H P Linder, A M Muasya, K C Oberlander, V Savolainen, D A Snijman, T Van Der Niet, T L Nowell, Phylogenet. Evol. 512009

Geographical affinities of the Cape flora, South Africa. C Galley, H P Linder, J. Biogeogr. 332006

The Cape element in the Afrotemperate flora: from Cape to Cairo?. C Galley, B Bytebier, D U Bellstedt, H P Linder, Proc. Roy. Soc. Lond. B. 2742007

Mining the mammalian genome for artiodactyl systematics. C A Matthee, J D Burzlaff, J F Taylor, S K Davis, Syst. Biol. 502001

Reciprocal chromosome painting among human, aardvark, and elephant (superorder Afrotheria) reveals the likely eutherian ancestral karyotype. F Yang, E Z Alkalaeva, P L Perelman, A T Pardini, W R Harrison, P C M O'brien, B Fu, A S Graphodatsky, M A Ferguson-Smith, T J Robinson, Proc. Natl. Acad. Sci. USA. 1002003

Phylogeny and biogeography of the genus Pseudobarbus (Cyprinidae): shedding light on the drainage history of rivers associated with the Cape Floristic Region. E R Swartz, P H Skelton, P Bloomer, Mol. Phylogenet. Evol. 512009

Dominant influence of HLA-B in mediating the potential co-evolution of HIV and HLA. P Kiepiela, A J Leslie, I Honeyborne, D Ramduth, C Thobakgale, S Chetty, P Rathnavalu, C Moore, K J Pfafferott, L Hilton, P Zimbwa, S Moore, T Allen, C Brander, M M Addo, M Altfeld, I James, S Mallal, M Bunce, L D Barber, J Szinger, C Day, P Klenerman, J Mullins, B Korber, H M Coovadia, B D Walker, P J R Goulder, Nature. 4322004

Searching for phylogenetic pattern in biological invasions. S Proches, J R U Wilson, D M Richardson, M Rejmanek, Glob. Ecol. Biogeogr. 172008

Rapid plant diversification: Planning for an evolutionary future. R M Cowling, R L Pressey, Proc. Natl. Acad. Sci. USA. 982001


Anemia in relation to body mass index and waist circumference among chinese women

Yu Qin
Alida Melse-Boonstra
Xiaoqun Pan
Baojun Yuan
Yue Dai
Jinkou Zhao
Michael B Zimmermann
Frans J Kok
Minghao Zhou
Zumin Shi
Anemia in relation to body mass index and waist circumference among chinese women
10.1186/1475-2891-12-10S H O R T R E P O R T Open Access
Background: This study aimed to investigate the relationship of anemia and body mass index among adult women in Jiangsu Province, China. Data were collected in a sub-national cross-sectional survey, and 1,537 women aged 20 years and above were included in the analyses. Subjects were classified by body mass index (BMI) categories as underweight, normal weight, overweight and obese according to the Chinese standard. Central obesity was defined as a waist circumference ≥ 80 cm. Anemia was defined as hemoglobin concentration < 12 g/dl. Prevalence ratios (PRs) of the relationship between anemia and BMI or waist circumference were calculated using Poisson regression. Findings: Overall, 31.1% of the Chinese women were anemic. The prevalence of overweight, obesity and central obesity was 34.2%, 5.8% and 36.2%, respectively. The obese group had the highest concentrations of hemoglobin compared with other BMI groups. After adjustment for confounders, overweight and obese women had a lower PR for anemia (PR: 0.72, 95% CI: 0.62-0.89; PR: 0.59, 95% CI: 0.43-0.79). Central obesity was inversely associated with anemia. Conclusion: In this Chinese population, women with overweight/obesity or central obesity were less likely to be anemic as compared to normal weight women. No measures are required currently to target anemia specifically for overweight and obese people in China.

Anemia can increase risk of maternal and child mortality, impair cognitive and physical development in children, and endanger physical performance in adults [1,2]. In China, 20% of preschool children and of nonpregnant women at reproductive age are affected by anemia [3], which can be classified as a moderate public health problem according to world health organization criteria (WHO) [2].

Obesity has been reported to be associated with anemia in adults in some countries [4][5][6][7][8][9][10], which may be due to up-regulated hepcidin expression thereby hampering iron absorption [11]. Therefore, obesity could potentially add to the burden of anemia in China, since the country has experienced an alarming increase in obesity-related chronic diseases over the past decade [12]. Therefore, we investigated the relationship between overall and central obesity with anemia among a female Chinese population.

Method and materials

The study was conducted in Jiangsu Province using a multistage cluster sampling method as described before [13], which was part of a national representative crosssectional study on Nutrition and Health conducted in 2002. The study was approved by the Human Investigation Review Committee at the National Institute for Nutrition and Food Safety, Chinese Center for Disease Control and Prevention. Written informed consent was obtained from the subject for publication of the data collected. Three towns and six counties were selected based on geographic directions and economic development. Three street/towns were randomly selected from each of the cities and counties. In each town/street, two villages/ neighborhoods were further randomly selected. In each village/neighborhood, 30 households were randomly selected. All members in the households were invited to take part in the study. Altogether, 1,537 out of 1,652 women with complete data were included in the survey. Energy and nutrient intake was calculated using three consecutive days of 24-h dietary recall in conjunction with the China Food Composition Table published in 2002 [14]. Anemia was defined as a hemoglobin concentration below 12 g/dl [1]. Women were classified by BMI categories as underweight (BMI < 18.5), normal weight (BMI > 18.5 < 24), overweight (BMI ≥ 24 < 28) and obesity (BMI ≥ 28) according to the Chinese standard. Central obesity was defined as a waist circumference ≥ 80 cm [15]. Low socio-economic status (SES) was defined as an annual income of less than 1,999 Yuan, 'medium' as 2,000-4,999 Yuan and 'high' as more than 5,000 Yuan.

Variables were presented as percentage or means ± standard deviations (SD) by BMI categories, with chisquare test for categorical variables and ANOVA for continuous variables. Poisson regression was used to estimate the association as prevalence ratios (PRs) between BMI categories, central obesity and anemia controlling for confounders, including age, residence, SES, educational level, and daily energy and iron intake.

Results

The mean age of the subjects was 46.4 ± 14.7 yrs. The average BMI was 23.6 ± 3.7. Table 1 presents general characteristics of the study population by BMI categories. Compared with underweight subjects, obese/overweight women had higher iron intake. Energy intake and hemoglobin concentration increased over BMI categories. The overall prevalence of anemia was 31.1%. Women with high and medium SES had higher prevalence of anemia than women with low SES (35.4% and 35.9% vs 21.5%, P < 0.001). No difference in prevalence of anemia was found for age, urban/rural and education level groups. Anemia showed a significant decreasing trend with increasing BMI. Compared to normal weight women, overweight and obese women had lower PRs for anemia (PR: 0.72, 95% CI: 0.62-0.89; PR: 0.59, 95% CI: 0.43-0.79). Central obesity was also inversely associated with anemia (PR: 0.75, 95% CI: 0.63-0.89).

Discussion

In this representative cross-sectional study, we found that both overweight/obesity and central obesity were inversely associated with anemia. The result was consistent with studies from Peru, Egypt, and the US, but not with a Mexican study [4,5]. The level of iron and vitamin C intake may partly explain the discrepancy. In our study, average iron intake ranged from 20 to 24 mg/d, which is in line with the Adequate Intake of 20 mg/d for Chinese women [16]. Although obese/overweight women had a higher intake of iron than underweight women, the average intake of underweight women was still adequate. In contrast, in the Mexican population iron intake was reported to be in the range of 8-9 mg/d [5]. Intake of vitamin C, the most potent enhancer of non-heme iron absorption, was present in sufficient amounts in the diets of Chinese women (60 mg/d), whereas vitamin C intake in Mexican women was low (30 mg/d). It may be that the Chinese diet conveys enough absorbable iron to lower the risk of anemia in contrast to the Mexican diet [6]. Although overweight or obesity in the population may not decrease red-cell survival or impair erythropoiesis, obesity might still result in hypoferremia through hepcidin or other mediators [4]. Waist circumference reflects intra-abdominal fat mass, and is related to cardiovascular diseases in adults [17]. Limited studies have assessed the relationship between central obesity and anemia. Gillum et al. [8] reported a positive association between waist-hip-ratio and serum ferritin. In our study, women with central obesity were less likely to have anemia, consistent with the results with overall obesity.

The main limitation of our study is that we used anemia as an indicator which only represents a part of the complex assessment of iron status. Therefore, we cannot truly distinguish anemia of chronic disease and anemia caused by iron deficiency.

In conclusion, in this study we found an inverse association between overweight/obesity, central obesity and anemia in Chinese women from Jiangsu Province. Our study contributes to the existing knowledge base on the complex association between adiposity and anemia. Inclusion of multiple iron and inflammation markers in future studies could possibly unravel the true meaning of our findings.

Table 1
1General characteristics of the study population (n = 1,537) by BMI categoriesUnderweight
Normal weight
Overweight
Obese
P value

n (%)
89 (5.8)
834 (54.3)
424 (27.6)
190 (12.4)

Age (years) (%)

< 35
38.2
29.5
16.5
9.5
< 0.001

35-44
13.5
25.4
21.9
21.6

45-54
13.5
19.9
33.7
26.3

≥ 55
34.8
25.2
27.8
42.6

Residence

Urban city
23.6
22.1
27.4
31.1
0.03

Rural city
76.4
77.9
72.6
68.9

Socio-economic status

Low
26.1
32.4
33.9
34.0
0.39

Medium
38.6
31.0
34.8
33.0

High
35.2
36.6
31.3
33.0

Education

Low
50.6
54.9
59.4
65.3
0.002

Medium
27.0
32.3
30.9
21.1

High
22.5
12.8
9.7
13.7

Hemoglobin (g/L) 1
125.0 (14.6)
124.9 (15.4)
128.4 (15.0)
131.9 (15.1)
< 0.001

Energy (kcal/d)
1916 (563)
2124 (582)
2179 (639)
2198 (637)
0.001

Iron (mg/d)
20.0 (7.4)
23.4 (9.6)
24.2 (9.8)
23.8 (9.5)
0.003

Vitamin C (mg/d)
61 (33)
61 (38)
59 (39)
60 (36)
0.886

1

Mean (SD), all such values; BMI, body mass index. Chi-square test for categorical variables and ANOVA for continuous variables.

http://www.nutritionj.com/content/12/1/10
AcknowledgementWe are extremely grateful to all the families who took part in this study. We thank the participating Regional Centers for Disease Control and Prevention in Jiangsu province, including the Nanjing, Xuzhou, Jiangyin, Taicang, Suining, Jurong, Sihong, and Haimen Centers for their support for the data collection.Competing interestsThe authors declare that they have no competing interests. The Project was supported by Jiangsu Provincial Health Bureau. Yu Qin is supported by an INREF fellowship from Wageningen University, the Netherlands. There are no financial competing interests.Authors' contribution YQ, contributed to the design, field work, data collection, analysis and manuscript writing. AMB, corresponding author, contributed to data interpretation and manuscript writing. XP, BY, YD, JZ, and MZ, contributed to the implementation in the field and gave advice on the manuscript writing. MBZ, FJK, and ZS, contributed to the overall scientific overview throughout the study and to manuscript writing. All authors read and approved the final manuscript.
World Health Organization: Iron deficiency anemia: assessment, prevention, and control. A guide for programme managers. Geneva: World Health Organization. World Health Organization: Iron deficiency anemia: assessment, prevention, and control. A guide for programme managers. Geneva: World Health Organization; 2001.

World Health Organization: Worldwide prevalence of anemia 1993-2005. WHO global database on Anemia. Geneva: World Health Organization. World Health Organization: Worldwide prevalence of anemia 1993-2005. WHO global database on Anemia. Geneva: World Health Organization; 2008.

Iron and zinc deficiencies in China: what is a feasible and cost-effective strategy? Public Health Nutr. G Ma, Y Jin, Y Li, F Zhai, F J Kok, E Jacobsen, X Yang, 11Ma G, Jin Y, Li Y, Zhai F, Kok FJ, Jacobsen E, Yang X: Iron and zinc deficiencies in China: what is a feasible and cost-effective strategy? Public Health Nutr 2008, 11(6):632-638.

Is obesity associated with anemia of chronic disease? a population-based study. K J Ausk, G N Ioannou, Obesity. 1610Silver SpringAusk KJ, Ioannou GN: Is obesity associated with anemia of chronic disease? a population-based study. Obesity (Silver Spring) 2008, 16(10):2356-2361.

Sharply higher rates of iron deficiency in obese mexican women and children are predicted by obesity-related inflammation rather than by differences in dietary iron intake. A C Cepeda-Lopez, S J Osendarp, A Melse-Boonstra, I Aeberli, F Gonzalez-Salazar, E Feskens, S Villalpando, M B Zimmermann, Am J Clin Nutr. 935Cepeda-Lopez AC, Osendarp SJ, Melse-Boonstra A, Aeberli I, Gonzalez- Salazar F, Feskens E, Villalpando S, Zimmermann MB: Sharply higher rates of iron deficiency in obese mexican women and children are predicted by obesity-related inflammation rather than by differences in dietary iron intake. Am J Clin Nutr 2011, 93(5):975-983.

The overlap of overweight and anaemia among women in three countries undergoing the nutrition transition. C L Eckhardt, L E Torheim, E Monterrubio, S Barquera, M T Ruel, Eur J Clin Nutr. 622Eckhardt CL, Torheim LE, Monterrubio E, Barquera S, Ruel MT: The overlap of overweight and anaemia among women in three countries undergoing the nutrition transition. Eur J Clin Nutr 2008, 62(2):238-246.

Weight status and iron deficiency among urban malian women of reproductive age. N Fanou-Fogny, Js N Koreissi, Y Amd R, A Melse-Boonstra, Db I, Br J Nutr. 1054Fanou-Fogny N, JS N, Koreissi Y, AMD R, Melse-Boonstra A, DB I: Weight status and iron deficiency among urban malian women of reproductive age. Br J Nutr 2011, 105(4):574-579.

Association of serum ferritin and indices of body fat distribution and obesity in Mexican American men-the third national health and nutrition examination survey. R F Gillum, Int J Obes Relat Metab Disord. 255Gillum RF: Association of serum ferritin and indices of body fat distribution and obesity in Mexican American men-the third national health and nutrition examination survey. Int J Obes Relat Metab Disord 2001, 25(5):639-645.

Iron and obesity in females in the United States. F Neymotin, U Sen, Obesity (Silver Spring). 191Neymotin F, Sen U: Iron and obesity in females in the United States. Obesity (Silver Spring) 2011, 19(1):191-199.

Poor iron status is not associated with overweight or overfat in non-obese pre-menopausal women. J P Karl, H R Lieberman, S J Cable, K W Williams, E L Glickman, A J Young, J P Mcclung, J Am Coll Nutr. 281Karl JP, Lieberman HR, Cable SJ, Williams KW, Glickman EL, Young AJ, McClung JP: Poor iron status is not associated with overweight or overfat in non-obese pre-menopausal women. J Am Coll Nutr 2009, 28(1):37-42.

Hepcidin expression in anemia of chronic disease and concomitant iron-deficiency anemia. P P Cheng, X Y Jiao, X H Wang, J H Lin, Y M Cai, Clin Exp Med. 111Cheng PP, Jiao XY, Wang XH, Lin JH, Cai YM: Hepcidin expression in anemia of chronic disease and concomitant iron-deficiency anemia. Clin Exp Med 2011, 11(1):33-42.

Is China facing an obesity epidemic and the consequences? The trends in obesity and chronic disease in China. Y Wang, J Mi, X Y Shan, Q J Wang, K Y Ge, Int J Obes. 311Wang Y, Mi J, Shan XY, Wang QJ, Ge KY: Is China facing an obesity epidemic and the consequences? The trends in obesity and chronic disease in China. Int J Obes 2007, 31(1):177-188.

Dietary intake of zinc in the population of Jiangsu Province, China. Y Qin, A Melse-Boonstra, Z Shi, X Pan, B Yuan, Y Dai, J Zhao, M B Zimmermann, F J Kok, M Zhou, Asia Pac J Clin Nutr. 182Qin Y, Melse-Boonstra A, Shi Z, Pan X, Yuan B, Dai Y, Zhao J, Zimmermann MB, Kok FJ, Zhou M: Dietary intake of zinc in the population of Jiangsu Province, China. Asia Pac J Clin Nutr 2009, 18(2):193-199.

Beijing: Beijing Medical University Publishing House. Y Yang, G Wang, X Pan, China Food Composition Table. Yang Y, Wang G, Pan X: China Food Composition Table 2002. Beijing: Beijing Medical University Publishing House; 2002.

Predictive values of body mass index and waist circumference for risk factors of certain related diseases in Chinese adults: study on optimal cut-off points of body mass index and waist circumference in Chinese adults. Z Bei-Fan, Asia Pac J Clin Nutr. 118SupplBei-Fan Z: Predictive values of body mass index and waist circumference for risk factors of certain related diseases in Chinese adults: study on optimal cut-off points of body mass index and waist circumference in Chinese adults. Asia Pac J Clin Nutr 2002, 11(Suppl 8):S685-S693.

Chinese Nutrition Association: Chinese Dietary Reference Intakes. Chinese Light Industry PressBeijingChinese Nutrition Association: Chinese Dietary Reference Intakes. Beijing: Chinese Light Industry Press; 2001.

Body mass index, waist circumference and waist-hip ratio: which is the better discriminator of cardiovascular disease mortality risk? Evidence from an individual-participant meta-analysis of 82 864 participants from nine cohort studies. S Czernichow, A P Kengne, E Stamatakis, M Hamer, G D Batty, 10.1186/1475-2891-12-10Obes Rev. 129Czernichow S, Kengne AP, Stamatakis E, Hamer M, Batty GD: Body mass index, waist circumference and waist-hip ratio: which is the better discriminator of cardiovascular disease mortality risk? Evidence from an individual-participant meta-analysis of 82 864 participants from nine cohort studies. Obes Rev 2011, 12(9):680-687. doi:10.1186/1475-2891-12-10

Anemia in relation to body mass index and waist circumference among chinese women. Qin, Nutrition Journal. 1210Cite this article asCite this article as: Qin et al.: Anemia in relation to body mass index and waist circumference among chinese women. Nutrition Journal 2013 12:10.