An assessment of trace element accumulation in palm oil production棕榈油生产中微量元素累积的评估

Review

Hadee Thompson-Morrison * , Sally Gaw and Brett Robinson

School of Physical and Chemical Sciences, University of Canterbury, Christchurch 8041, New Zealand; sally.gaw@canterbury.ac.nz (S.G.); brett.robinson@canterbury.ac.nz (B.R.)

* Correspondence: hadee.thompson-morrison@protonmail.com

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Academic Editor: Domenico Ronga

Received: 22 February 2022 Accepted: 7 April 2022 Published: 11 April 2022

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Copyright: © 2022 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https:// creativecommons.org/licenses/by/ 4.0/).

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Abstract: African oil palm (Elaeis guineensis) is grown on 17,000,000 hectares in Southeast Asia, producing oil and the by-product, palm kernel expeller (PKE), for export. Elaeis guineensis is typically produced on weathered acidic soils, with fertilisers and fungicides used to increase production. These amendments can contain elevated concentrations of trace elements (TEs), either as the active ingredient (e.g., Cu-based fungicides) or as contaminants, including F, Zn, As, Cd, Pb and U. TEs may accumulate in soil over time, and be taken up by plants, posing a food-chain transfer risk if allowed to exceed soil guideline values. We reviewed available literature on trace elements in soil, plant material, oil and PKE to evaluate the risk of TE accumulation due to phosphate fertiliser and Cu-fungicide use. TE concentrations of Cu, Zn, and Cd were reported to be up to 69, 107 and 5.2 mg kg⁻¹, respectively, in E. guineensis plantation soils, while Cu and As were reported to be up to 28.9 and 3.05 mg kg⁻¹, respectively, in PKE (>50% their permissible limits). Iron, a TE, has also been reported in PKE up to 6130 mg kg⁻¹ (>10-fold the permissible limit). TE accumulation is an emerging issue for the palm oil industry, which, if unaddressed, will negatively affect the industry’s economic and environmental sustainability. There are critical knowledge gaps concerning TEs in palm oil systems, including a general lack of research from Southeast Asian environments and information concerning key contaminants (Fe, Cu, As and Cd) in soils, plants and PKE.

摘要：非洲油棕（Elaeis guineensis）在东南亚的种植面积达17,000,000 ha，其产出的棕榈油及副产品棕榈仁粕（palm kernel expeller，PKE）主要用于出口。Elaeis guineensis通常种植于风化程度高的酸性土壤上，需施用化肥和杀菌剂以提高产量。这些投入品可能含有较高浓度的微量元素（TEs），它们或作为有效成分（如铜基杀菌剂），或作为污染物存在，包括F、Zn、As、Cd、Pb和U。微量元素可随时间在土壤中累积并被植物吸收，若超过土壤指导值，则存在沿食物链传递的风险。本文综述了有关土壤、植物材料、油脂及PKE中微量元素的现有文献，以评估施用磷肥和铜基杀菌剂导致微量元素累积的风险。据报道，E. guineensis种植园土壤中Cu、Zn和Cd的浓度分别高达69、107和5.2 mg kg⁻¹，而PKE中Cu和As的浓度分别高达28.9和3.05 mg kg⁻¹（超过其允许限值的50%）。作为一种微量元素，PKE中Fe的浓度亦有高达6130 mg kg⁻¹的报道（超过允许限值10倍以上）。微量元素累积是棕榈油产业面临的一个新问题，若不加以解决，将对该产业的经济和环境可持续性产生不利影响。目前有关棕榈油生产体系中微量元素的研究存在关键的知识空白，包括普遍缺乏针对东南亚环境的研究，以及缺乏土壤、植物和PKE中主要污染物（Fe、Cu、As和Cd）的相关信息。

Keywords: copper; Elaeis guineensis; fertiliser contaminants; heavy metals; palm kernel expeller

关键词：铜；Elaeis guineensis；化肥污染物；重金属；棕榈仁粕

1Introduction引言

The African oil palm (Elaeis guineensis Jacq.) is the highest yielding oil crop, with a maximum potential yield of 8 t ha⁻¹ [1]. From 2012–2020, E. guineensis represented 36–37% of vegetable oil production worldwide [2,3]. Indonesia and Malaysia supply ca. 85% of the world’s palm oil, with a combined harvestable area of more than 17,000,000 ha [4,5]. Thailand, Colombia and Nigeria are the third-, fourth- and fifth-highest producing countries of palm oil, respectively [6]. Palm oil is used in products for health care, home care and hygiene, as well as in many processed foods [7]. A dry matter by-product of palm oil production, palm kernel expeller (PKE), is sold as a supplementary stockfeed. In 2020, worldwide PKE production reached 10,214,000 t [8].

非洲油棕（Elaeis guineensis Jacq.）是产量最高的油料作物，最大潜在产量可达8 t ha⁻¹ [1]。2012–2020年间，E. guineensis占全球植物油产量的36–37% [2,3]。印度尼西亚和马来西亚供应了全球约85%的棕榈油，两国可收获面积合计超过17,000,000 ha [4,5]。泰国、哥伦比亚和尼日利亚分别为棕榈油产量第三、第四和第五的国家 [6]。棕榈油被用于医疗保健、家居护理和卫生用品，以及多种加工食品中 [7]。棕榈油生产的干物质副产品棕榈仁粕（PKE）作为补充饲料出售。2020年，全球PKE产量达10,214,000 t [8]。

Production of E. guineensis in Southeast Asia occurs on tropical soils, which are typically weathered and acidic, and, as such, require significant fertiliser inputs to meet nutrient demands. Fungicides are applied to control plant disease [9–11]. Without fertiliser applications of Nitrogen (N), Phosphorus (P), Potassium (K), Magnesium (Mg) and Boron (B), E. guineensis trees will become nutrient deficient, yields will decline, and production may become uneconomic, particularly for smallholders in Southeast Asian environments [11,12]. Applications of Copper (Cu) and Zinc (Zn) are also critical when growing E. guineensis on Histosol soils [11]. Fertiliser trials have shown that yields may reach 8 t oil ha⁻¹ yr⁻¹ with appropriate fertiliser management; however, the average yield is 4 t ha⁻¹ yr⁻¹ [1,13,14]. Fungicidal treatments using Cu as an active ingredient are commonly applied to prevent plant diseases, including Ganoderma spp. [15]. Fertilizers and fungicides can contain significant concentrations of trace elements (TEs), either as part of the active ingredient [16] or as a contaminant [17]. TE contaminants in agrichemicals can accumulate in soil [18], which can result in reduced soil fertility [19] and/or uptake into the (human) food chain [20,21].

东南亚E. guineensis的生产在热带土壤上进行，这些土壤通常风化程度高且呈酸性，因此需要大量施肥以满足养分需求。此外还需施用杀菌剂以防治植物病害 [9–11]。若不施用氮（N）、磷（P）、钾（K）、镁（Mg）和硼（B）肥，E. guineensis植株将出现养分缺乏，产量下降，生产可能变得不经济，对东南亚环境中的小农户而言尤其如此 [11,12]。在有机土（Histosol）上种植E. guineensis时，施用铜（Cu）和锌（Zn）也至关重要 [11]。施肥试验表明，在合理的施肥管理下，产量可达8 t 油 ha⁻¹ yr⁻¹；然而平均产量仅为4 t ha⁻¹ yr⁻¹ [1,13,14]。以Cu为有效成分的杀菌剂处理常被用于防治植物病害，包括Ganoderma spp.（灵芝属真菌）[15]。化肥和杀菌剂中可能含有相当浓度的微量元素（TEs），它们或作为有效成分的一部分 [16]，或作为污染物存在 [17]。农用化学品中的微量元素污染物可在土壤中累积 [18]，进而导致土壤肥力下降 [19]和/或进入（人类）食物链 [20,21]。

A combination of poor environmental controls (in the form of poor monitoring and enforcement of fertiliser-use recommendations) and a lack of knowledge about soil nutrient status and plant requirements often leads to inappropriate fertiliser applications, particularly in Southeast Asian smallholder plantations [22]. As well as having demonstrable negative effects on fruit-bunch yield [12], inefficient nutrient management can lead to the contamination of soils and surface and groundwaters due to N leaching or the run-off of P and TEs [23]. Similarly, TE-containing fungicides may be overapplied, accelerating TE accumulation in soil. Cadmium (Cd) from fertilisers and Cu from fungicides are two of the most likely TE contaminants to accumulate in horticultural soils [24,25]; however, other fertiliser-borne contaminants include Fluorine (F), Chromium (Cr), Zn, Arsenic (As) and Lead (Pb) [17].

环境管控不力（表现为对化肥使用建议的监测和执行不到位）以及对土壤养分状况和植物需求缺乏了解，常常导致不当施肥，这在东南亚小农户种植园中尤为突出 [22]。低效的养分管理不仅对果串产量具有明显的负面影响 [12]，还可能因N的淋溶或P和微量元素的径流而导致土壤、地表水和地下水污染 [23]。同样，含微量元素的杀菌剂也可能被过量施用，从而加速微量元素在土壤中的累积。来自化肥的镉（Cd）和来自杀菌剂的Cu是园艺土壤中最可能累积的两种微量元素污染物 [24,25]；然而，其他源自化肥的污染物还包括氟（F）、铬（Cr）、Zn、砷（As）和铅（Pb）[17]。

While there are disparate reports on TE concentrations in some components of E. guineensis production, there is no information available on fluxes throughout the whole system. This review aims to identify key TEs of concern, elemental fluxes, potential risks to ecosystems and human health, and knowledge gaps concerning this production system.

尽管已有零散报道涉及E. guineensis生产中某些组分的微量元素浓度，但尚无关于整个体系中元素通量的信息。本综述旨在识别该生产体系中需关注的主要微量元素、元素通量、对生态系统和人体健康的潜在风险以及知识空白。

2Trace Elements in Soils of Elaeis guineensis ProductionElaeis guineensis生产土壤中的微量元素

2.1. Sources of Trace Elements in Elaeis guineensis Plantation Soils2.1. Elaeis guineensis种植园土壤中微量元素的来源

2.1.1. Geogenic Trace Elements2.1.1. 地质成因微量元素

Soils naturally contain TEs, with concentrations varying geographically due to biogeochemical processes [26]. In tropical regions, weathering and climate are key factors influencing background TE concentrations of soils [27,28]. Food-chain transfer risk may occur when naturally high TE soils with low pH and organic matter content are used to produce food crops, as these conditions favour TE mobility and subsequent plant uptake [29,30]. Elaeis guineensis in Southeast Asia is typically cultivated on acidic, weathered soils, including Ultisols, Inceptisols, and Oxisols, as well as Histosols [11] according to the USDA Soil Classification [31]. Ultisols and Oxisols are generally highly leached and contain TEs, including Cobalt (Co), Nickel (Ni), Cu, Zn, Cd, Mercury (Hg) and Pb [32]. General background concentrations of these TEs in soils are 8, 40, 20, 50, 0.06, 0.03 and 10 mg kg⁻¹, respectively [26]. Histosols contain TEs (Titanium (Ti), Manganese (Mn), F and Barium (Ba) at background concentrations of 5000, 850, 200 and 500 mg kg⁻¹, respectively [26,33], which are released as the soil degrades under drainage and cultivation processes [34].

土壤天然含有微量元素，由于生物地球化学过程的作用，其浓度存在地理差异 [26]。在热带地区，风化作用和气候是影响土壤微量元素背景浓度的关键因素 [27,28]。当利用天然微量元素含量高、pH和有机质含量低的土壤生产粮食作物时，可能存在食物链传递风险，因为这些条件有利于微量元素的迁移及随后的植物吸收 [29,30]。根据USDA土壤分类系统 [31]，东南亚的Elaeis guineensis通常种植于酸性、风化的土壤上，包括老成土（Ultisols）、始成土（Inceptisols）、氧化土（Oxisols）以及有机土（Histosols）[11]。老成土和氧化土通常经历了强烈淋溶，含有钴（Co）、镍（Ni）、Cu、Zn、Cd、汞（Hg）和Pb等微量元素 [32]。这些微量元素在土壤中的一般背景浓度分别为8、40、20、50、0.06、0.03和10 mg kg⁻¹ [26]。有机土含有钛（Ti）、锰（Mn）、F和钡（Ba）等微量元素，其背景浓度分别为5000、850、200和500 mg kg⁻¹ [26,33]，这些元素在排水和耕作过程中随土壤退化而释放 [34]。

2.1.2. Anthropogenic Sources of Trace Elements in Soils2.1.2. 土壤中微量元素的人为来源

Most TEs that enter soils via agrichemical use are rapidly immobilised through the processes of specific absorption, occlusion and precipitation [35]. Therefore, most TEs will accumulate in soil following repeated applications of agrichemicals. TEs may be lost from the soil via surface erosion or run-off, while leaching of TEs is usually negligible [36].

通过施用农用化学品进入土壤的大多数微量元素会经由专性吸附、包蔽和沉淀等过程迅速被固定 [35]。因此，在反复施用农用化学品后，大多数微量元素将在土壤中累积。微量元素可通过地表侵蚀或径流从土壤中流失，而微量元素的淋溶通常可以忽略不计 [36]。

Tropical soils in Southeast Asia typically contain deficient levels of P to support E. guineensis production, thus requiring fertiliser inputs to provide plants with the required nutrients [11,37]. A study of smallholder plantations in Indonesia by Woittiez et al. [22] identified that Indonesian farmers relied heavily on subsidised fertilisers, which did not supply soils with appropriate nutrients for E. guineensis production. More than 99% of smallholders surveyed used mineral fertilisers, including several phosphatic fertilisers. These fertilisers can contain contaminants including F, Cu, Zn, As, Cd, Pb and Uranium (U), which can result in soil contamination and human exposure risk if inappropriately or excessively applied [17,38]. Rare earth elements (REEs) are also present in phosphate fertilisers and may enter the soil-plant system through regular use of these [39,40]. The rate of use and application of the most commonly used fertilisers reported by Woittiez et al.

东南亚热带土壤中的P含量通常不足以支撑E. guineensis的生产，因此需要施肥为植物提供所需养分 [11,37]。Woittiez et al. [22]对印度尼西亚小农户种植园的研究发现，印度尼西亚农民严重依赖补贴化肥，而这些化肥并不能为E. guineensis生产提供适宜的土壤养分。受访小农户中超过99%使用矿物肥料，其中包括多种磷肥。这些化肥可能含有F、Cu、Zn、As、Cd、Pb和铀（U）等污染物，若施用不当或过量，可导致土壤污染和人体暴露风险 [17,38]。磷肥中还含有稀土元素（REEs），经常施用磷肥可使其进入土壤–植物系统 [39,40]。Woittiez et al.报道的最常用化肥的使用率和施用量

are presented in Table 1, as well as the average mass of key elements added as fertiliser contaminants through such applications.

列于表1，同时列出了此类施肥过程中作为化肥污染物带入的主要元素的平均质量。

^a Calculated using average total contaminant concentrations in phosphate fertilisers from Taylor et al. [38]. ^b Possible range given due to the differing contaminant concentrations of Cd in phosphate rock dependent on geographical origin (20–200 mg Cd kg P2O5⁻¹ in sedimentary rock [41]).

^a 根据Taylor et al. [38]报道的磷肥中污染物平均总浓度计算。^b 由于磷矿石中Cd的污染浓度因地理来源而异（沉积岩中为20–200 mg Cd kg P2O5⁻¹ [41]），故给出可能的范围。

The majority of smallholders surveyed by Woittiez et al. [22] applied excessive amounts of fertilisers compared with the nutritional requirements of the crop and employed practices likely to lead to nutrient run-off and leaching. Such practices included weed-clearing in plantations using glyphosate and paraquat, which left soil bare and vulnerable to erosion and transfer to kernels. Farmers also manually (un-uniformly) mixed straight fertilisers, applied fertilisers in bulk once per year, and applied fertilisers in a narrow ring around the base of the palm, rather than uniformly to the soil area colonised by palm roots or on top of decomposing palm fronds, as is recommended as good practice [42–44]. Conversely, some farmers applied insufficient fertilisers for E. guineensis production (18% applied no K, 20% no P, and 15% no N), leading to decreased yield and soil nutrient deficiencies. Smallholders manage more than 40% of E. guineensis plantations in Indonesia (4,700,000 ha) [45], and inefficient nutrient management over this area is both a significant risk to the economic sustainability of this industry as well as a driver of deforestation, as more land area is needed to produce economically viable yields [22].

Woittiez et al. [22]调查的大多数小农户施肥量超出了作物的营养需求，并且采用了可能导致养分径流和淋溶的做法。这些做法包括在种植园中使用草甘膦和百草枯除草，使土壤裸露，易受侵蚀并向果仁迁移。农民还以人工（不均匀）方式混合单质肥料，每年一次性集中施肥，并将肥料施于棕榈树基部周围的狭窄环带内，而不是按照良好实践的建议均匀施于棕榈根系分布的土壤区域或正在分解的棕榈叶上 [42–44]。相反，也有部分农民对E. guineensis生产的施肥量不足（18%未施K，20%未施P，15%未施N），导致产量下降和土壤养分缺乏。小农户管理着印度尼西亚超过40%的E. guineensis种植园（4,700,000 ha）[45]，在如此大面积上的低效养分管理不仅对该产业的经济可持续性构成重大风险，而且由于需要更多土地才能获得经济上可行的产量，还成为毁林的驱动因素 [22]。

Elaeis guineensis production can be reduced by diseases; in particular, the fungal pathogen Ganoderma spp., which causes trunk rot, is especially problematic in Southeast Asian plantations [9,10,46]. Copper-based fungicides are commonly employed to control this disease, with available products having varying active ingredient (Cu) concentrations from 7.6–75% [10,15,47]. Bivi et al. [15] found that continuous Cu applications totalling 21.45 g Cu ha⁻¹ yr⁻¹ (combined with Calcium (Ca) and salicylic acid) were effective in controlling basal stem rot in E. guineensis plants (This application rate was calculated using data from Bivi et al. [15] with a tree density of 143 trees ha⁻¹, described as optimal by FAO [48]). However, the actual application rates used by farmers may be in excess of this due to the uncontrolled nature of fungicide use in Indonesia [49]. There is a lack of data available on actual Cu application rates utilised in E. guineensis plantations. In Europe, past fungicide application rates have been as high as 80 kg Cu ha⁻¹ on agricultural soils and have led to soil contamination [50]. Current European Union guidelines allow for applications of 6 kg Cu ha⁻¹ on agricultural soils [51]. Only one Indonesian study on fungicide use could be found for comparison [49]. Here, fungicide application rates used in hot pepper cultivation in Indonesia are reported as a mean of 14.3 kg active ingredient ha⁻¹ and a maximum of 33.8 kg active ingredient ha⁻¹. Copper was an active ingredient in the fungicides used in this study [52]. The variation in application rates observed in this study fits with that observed throughout other systems: for example, Morgan and Taylor [53] reported median Cu application rates of 2 kg ha⁻¹ yr⁻¹, with the highest application rate being 16 kg ha⁻¹ yr⁻¹ in New Zealand vineyards. Repeated applications of Cu-containing products to horticultural crops can result in Cu accumulation in soils [54,55] through the return of fungicide-applied plant material to the soil surface and through spray drift landing on the soil surface during application. In excessive quantities, Cu in soils can inhibit plant growth and pose risks to human health [56,57].

Elaeis guineensis的产量可能因病害而降低；特别是引起树干腐烂的真菌病原体Ganoderma spp.，在东南亚种植园中尤为严重 [9,10,46]。铜基杀菌剂常用于防治该病害，现有产品的有效成分（Cu）浓度为7.6–75%不等 [10,15,47]。Bivi et al. [15]发现，连续施用总量为21.45 g Cu ha⁻¹ yr⁻¹的Cu（与钙（Ca）和水杨酸配合使用）可有效防治E. guineensis植株的基腐病（该施用量根据Bivi et al. [15]的数据，按FAO [48]所述的最佳种植密度143株 ha⁻¹计算）。然而，由于印度尼西亚杀菌剂使用缺乏管控 [49]，农民的实际施用量可能超过该值。目前缺乏E. guineensis种植园实际Cu施用量的数据。在欧洲，农业土壤上过去的杀菌剂施用量曾高达80 kg Cu ha⁻¹，并已导致土壤污染 [50]。现行欧盟指南允许在农业土壤上施用6 kg Cu ha⁻¹ [51]。仅能找到一项关于杀菌剂使用的印度尼西亚研究可供比较 [49]。该研究报道，印度尼西亚辣椒种植中杀菌剂的施用量平均为14.3 kg 有效成分 ha⁻¹，最高为33.8 kg 有效成分 ha⁻¹。该研究所用杀菌剂中Cu为有效成分之一 [52]。该研究中观察到的施用量差异与其他体系中的情况一致：例如，Morgan and Taylor [53]报道新西兰葡萄园的Cu施用量中位数为2 kg ha⁻¹ yr⁻¹，最高施用量为16 kg ha⁻¹ yr⁻¹。在园艺作物上反复施用含Cu产品，可通过喷施过杀菌剂的植物材料返回土壤表面以及施药时飘移的雾滴落到土壤表面，导致Cu在土壤中累积 [54,55]。土壤中过量的Cu可抑制植物生长，并对人体健康构成风险 [56,57]。

2.2. Measured Trace Element Concentrations in Soil2.2. 土壤中微量元素的实测浓度

Available data on trace element concentrations in E. guineensis plantation soils are presented in Table 2. Two soils from Papua New Guinean E. guineensis plantations have Cd concentrations <1 mg kg⁻¹ [58]. Aini Azura et al. [59] reported Zn and Cd concentrations up to 99 and 5.2 mg kg⁻¹, respectively, in Malaysian E. guineensis production soils. These are the only two studies to be identified which were conducted in Southeast Asia, and thus there is a lack of relevant research looking at critical TEs, including F, Cu and Pb, in a Southeast Asian environment.

E. guineensis种植园土壤中微量元素浓度的现有数据列于表2。巴布亚新几内亚两处E. guineensis种植园土壤的Cd浓度 <1 mg kg⁻¹ [58]。Aini Azura et al. [59]报道，马来西亚E. guineensis生产土壤中Zn和Cd的浓度分别高达99和5.2 mg kg⁻¹。这是仅有的两项在东南亚开展的研究，因此缺乏在东南亚环境中针对F、Cu和Pb等关键微量元素的相关研究。

In Nigeria, TEs have been reported present in concentrations that both exceed and fall short of optimal concentrations for E. guineensis cultivation. Orobator et al. [60] reported significant differences in Mn, Iron (Fe), and Cd concentrations across three plantation sites, with Cu and Zn found to be deficient at one site and no excessive TE concentrations observed. In a separate study, E. guineensis plantation soil reportedly contained lower concentrations of Cu and Zn than secondary forest soils [61]. Soil Cr and Pb concentrations have been reported at background levels by Uwumarongie-Ilori et al. [62]. In contrast to these studies, Olafisoye et al. [63] reported Cd concentrations exceeding background concentrations (0.5 mg kg⁻¹) in 15 plantation soils, with the highest soil containing 4.3 mg kg⁻¹ Cd. This was attributed to the repeated use of phosphate fertilisers. Additionally, the authors reported that total Cr, Co, Ni and Pb concentrations exceeded maximum permissible levels for soils (100, 8, 40, and 10 mg kg⁻¹, respectively). The maximum reported soil copper concentration was 61 mg kg⁻¹ and was concluded to pose a toxicity risk to plants and animals. Elaeis guineensis production soils in Ghana were reported as Molybdenum (Mo) deficient by Golow et al. [64]. In all studies mentioned here, soil TE levels were found to be either deficient (Cu, Zn, Mo) or excessive (Cr, Co, Ni, Cu, Cd, Pb) relative to the requirement and tolerance of E. guineensis. This underlines the need to match on-farm management with soil status, especially in systems with high nutrient demands, such as palm cultivation on weathered tropical soils. Notably, no data could be found on F, As, or U concentrations in soil under E. guineensis production.

在尼日利亚，已有报道的微量元素浓度既有超过也有低于E. guineensis种植最适浓度的情况。Orobator et al. [60]报道三个种植园样点间Mn、铁（Fe）和Cd浓度存在显著差异，其中一个样点Cu和Zn缺乏，未观察到微量元素浓度过高的情况。另一项研究报道，E. guineensis种植园土壤中Cu和Zn的浓度低于次生林土壤 [61]。Uwumarongie-Ilori et al. [62]报道土壤Cr和Pb浓度处于背景水平。与上述研究相反，Olafisoye et al. [63]报道15个种植园土壤的Cd浓度超过背景浓度（0.5 mg kg⁻¹），其中最高者含Cd 4.3 mg kg⁻¹，这被归因于反复施用磷肥。此外，作者报道总Cr、Co、Ni和Pb浓度超过了土壤最大允许水平（分别为100、8、40和10 mg kg⁻¹）。报道的土壤铜最高浓度为61 mg kg⁻¹，并被认为对植物和动物存在毒性风险。Golow et al. [64]报道加纳的Elaeis guineensis生产土壤缺钼（Mo）。在上述所有研究中，相对于E. guineensis的需求和耐受性，土壤微量元素水平要么缺乏（Cu、Zn、Mo），要么过量（Cr、Co、Ni、Cu、Cd、Pb）。这凸显了农场管理须与土壤状况相匹配的必要性，尤其是在养分需求高的体系中，如在风化的热带土壤上种植棕榈。值得注意的是，未能找到E. guineensis生产土壤中F、As或U浓度的任何数据。

^a [26]. ^b Nigeria [60]. ^c Nigeria, range of means [63]. ^d Ghana, 0–40 cm depth [64]. ^e Nigeria [61]. ^f Malaysia [59]. ^g Papua New Guinea [58]. ^h X denotes an order of magnitude estimate.

^a [26]。^b 尼日利亚 [60]。^c 尼日利亚，均值范围 [63]。^d 加纳，0–40 cm深度 [64]。^e 尼日利亚 [61]。^f 马来西亚 [59]。^g 巴布亚新几内亚 [58]。^h X表示数量级估计值。

The TE concentrations in the aforementioned reports will be a function of both the agrichemicals used and the time that the land has been under agricultural production, either as E. guineensis or a previous crop(s). Given that many E. guineensis plantations have recently been converted from virgin forests, TE concentrations may still be similar to background levels. Therefore we might hypothesise that TE concentrations in African soils, which were converted to E. guineensis some 100 years ago [13], will have higher TE concentrations than recently converted soils in Southeast Asia.

上述报道中的微量元素浓度既取决于所使用的农用化学品，也取决于土地用于农业生产（无论是种植E. guineensis还是之前的作物）的时间长短。鉴于许多E. guineensis种植园是近期由原始森林转化而来，其微量元素浓度可能仍与背景水平相近。因此我们可以推测，约100年前即已转为种植E. guineensis的非洲土壤 [13]，其微量元素浓度将高于东南亚近期转化的土壤。

3Trace Elements in Elaeis guineensis and Comparable SpeciesElaeis guineensis及相近物种中的微量元素

There are three varieties of E. guineensis: pisifera, dura, and the hybrid variety tenera [65]. Var. pisifera typically has no endocarp and a thick mesocarp, var. dura a thick mesocarp and endocarp, and var. tenera a moderately thick mesocarp and thin endocarp, with a moderately sized endosperm [13]. This hybrid variety was developed to produce higher oil-yielding crops and now dominates most plantations in Southeast Asia [66].

E. guineensis有三个变种：pisifera、dura及杂交变种tenera [65]。Var. pisifera通常无内果皮，中果皮厚；var. dura中果皮和内果皮均厚；var. tenera中果皮中等厚度，内果皮薄，胚乳大小中等 [13]。该杂交变种是为获得更高的产油量而培育的，目前在东南亚大多数种植园中占主导地位 [66]。

Monocotyledonous plants, including E. guineensis, uptake TEs from soil via exchange sites on root surfaces that are then transported to the above-ground portions, especially the leaves, via xylem transport, using the symplastic and apoplastic pathways. Leaf tissue, a water sink, is expected to have higher concentrations of TEs relative to other tissue. To reach the fruit, however, TEs must be transported in the phloem and maybe traverse the placenta, making fruit tissues (mesocarp and seed) likely to contain lower TE concentrations [67]. In E. guineensis production systems, leaves (fronds) are often returned to soil as organic matter inputs [68,69]. If high levels of TEs are contained within these leaves, or if TEs are sorbed to palm fronds after fungicide spray applications, this may result in accumulation of TEs on the soil surface following leaf abscission. The study mentioned in Section 2.2 by Aini Azura et al. [56] is the only study that could be identified which investigated TE concentrations in E. guineensis fronds, reporting concentrations of ca. 0.18–0.38 mg kg⁻¹ for Cd and ca. 15–28 mg kg⁻¹ for Zn.

包括E. guineensis,在内的单子叶植物通过根表面的交换位点从土壤中吸收微量元素，随后经由共质体和质外体途径，通过木质部运输转运至地上部分，尤其是叶片。叶片组织作为水分汇，预计其微量元素浓度高于其他组织。然而，微量元素须经韧皮部运输并可能穿过胎座才能到达果实，因此果实组织（中果皮和种子）的微量元素浓度可能较低 [67]。在E. guineensis生产体系中，叶片（棕榈叶）常作为有机质投入物归还土壤 [68,69]。若这些叶片中含有高水平的微量元素，或微量元素在喷施杀菌剂后吸附于棕榈叶上，则叶片脱落后可能导致微量元素在土壤表面累积。2.2节中提到的Aini Azura et al. [56]的研究是唯一能找到的调查E. guineensis棕榈叶中微量元素浓度的研究，报道的Cd浓度约为0.18–0.38 mg kg⁻¹，Zn浓度约为15–28 mg kg⁻¹。

Only three relevant studies could be identified which addressed TE concentrations in E. guineensis kernels. Nigerian kernels were generally reported to contain higher levels of Mn, Fe, Cu and Zn (up to 610, 220, 26 and 43 mg kg⁻¹, respectively) relative to Malaysian kernels (up to 145, 52, 18 and 36 mg kg⁻¹, respectively) [70,71]. Lead was reported below detection levels in Nigerian kernels, while Cd was reported up to ca. 0.31 mg kg⁻¹ in Malaysian kernels [59,71]. Mean concentrations of TEs in E. guineensis kernels from these studies are compared with average TE concentrations of land plants in Table 3.

仅能找到三项涉及E. guineensis果仁中微量元素浓度的相关研究。据报道，尼日利亚果仁中Mn、Fe、Cu和Zn的含量（分别高达610、220、26和43 mg kg⁻¹）总体高于马来西亚果仁（分别高达145、52、18和36 mg kg⁻¹）[70,71]。尼日利亚果仁中Pb低于检出限，而马来西亚果仁中Cd高达约0.31 mg kg⁻¹ [59,71]。表3将这些研究中E. guineensis果仁的微量元素平均浓度与陆生植物的平均微量元素浓度进行了比较。

^a [26]. ^b Endosperm of seed- and clonally-derived var. tenera [70]. ^c Defatted and undefatted var. tenera and var. dura [71]. ^d Estimated from graph [59].

^a [26]。^b 种子繁殖和克隆繁殖的var. tenera的胚乳 [70]。^c 脱脂和未脱脂的var. tenera和var. dura [71]。^d 根据图表估算 [59]。

While research on TEs in E. guineensis plant material is sparse, data have been collected on TEs in other Arecaceae species, including date palm (Phoenix dactylifera L.), acai (Euterpe oleracea Mart.), and jucara (Euterpe edulis Mart.) (Table 4). Due to their similar physiologies, TEs in these species may behave similarly to those in E. guineensis. As such, it is beneficial here to review the literature concerning TEs in these Arecaceae species to garner insights into whether a wider range of TEs may accumulate in E. guineensis.

尽管关于E. guineensis植物材料中微量元素的研究很少，但已有关于其他棕榈科（Arecaceae）物种中微量元素的数据，包括海枣（Phoenix dactylifera L.）、巴西莓（Euterpe oleracea Mart.）和jucara（Euterpe edulis Mart.）（表4）。由于生理特性相似，这些物种中微量元素的行为可能与E. guineensis中的相似。因此，有必要在此综述有关这些棕榈科物种中微量元素的文献，以了解E. guineensis.中是否可能累积更广泛的微量元素。

^a Spain [72]. ^b Pakistan, number in brackets assumed to be standard deviation of the mean, n ≥ 6 [73]. ^c Turkey, range of means [76]. ^d [74]. ^e Saudi Arabia, range of means [75]. ^f [40].

^a 西班牙 [72]。^b 巴基斯坦，括号内数字假定为平均值的标准差，n ≥ 6 [73]。^c 土耳其，均值范围 [76]。^d [74]。^e 沙特阿拉伯，均值范围 [75]。^f [40]。

Accumulation of Cr, Co and Ni has been reported in mesocarp and seed up to concentrations of 0.5, 5.1 and 0.7 mg kg⁻¹, respectively [72]. In a separate study, As was reported in mesocarp samples at 0.17 mg kg⁻¹, although this did not exceed tolerable dietary levels [73]. Comparable concentrations were reported for Cd in P. dactylifera and E. oleracea, of up to 0.13 and 0.0094 mg kg⁻¹, respectively [72,74]. Both leaves and mesocarp of P. dactylifera have been shown to take up TEs from the air in contaminated environments, with TE concentrations increasing in areas with increased anthropogenic air pollution sources [75,76].

已有报道表明，中果皮和种子中Cr、Co和Ni的累积浓度分别高达0.5、5.1和0.7 mg kg⁻¹ [72]。另一项研究报道中果皮样品中As为0.17 mg kg⁻¹，但未超过可耐受的膳食水平 [73]。P. dactylifera和E. oleracea中Cd的报道浓度相近，分别高达0.13和0.0094 mg kg⁻¹ [72,74]。研究表明，在受污染环境中P. dactylifera的叶片和中果皮均可从空气中吸收微量元素，且在人为大气污染源增加的区域其微量元素浓度随之升高 [75,76]。

Rare earth element concentrations of E. oleracea and E. edulis were reported by Santos et al. [40]. Euterpe oleracea contained the highest concentrations of REEs, up to 230, 575 and 179 mg kg⁻¹ for La, Ce and Th, respectively. It was also reported that geographical location affected REE concentrations of both E. oleracea and E. edulis. This emphasises the variation which can occur in the TE content of plant tissues due to geographical and geological factors. Tables of REE contents in Arecaceae species are provided in the Supplementary Materials.

Santos et al. [40]报道了E. oleracea和E. edulis中的稀土元素浓度。Euterpe oleracea的稀土元素浓度最高，La、Ce和Th分别高达230、575和179 mg kg⁻¹。该研究还报道，地理位置影响E. oleracea和E. edulis的稀土元素浓度。这突出表明，地理和地质因素可导致植物组织中微量元素含量产生差异。棕榈科物种稀土元素含量表见补充材料。

The TE concentrations detailed in Table 4 indicate that TE accumulation occurs in palm species when exposure pathways are present. This indicates that TE accumulation in E. guineensis tissues and associated products may occur when plants are grown in contaminated environments.

表4中详列的微量元素浓度表明，当存在暴露途径时，棕榈类物种会发生微量元素累积。这说明当植株生长于受污染环境中时，E. guineensis组织及相关产品中可能发生微量元素累积。

4Trace Elements in Palm Oils棕榈油中的微量元素

The E. guineensis tree produces two types of oil from its fruit: palm kernel oil from the endosperm; and palm oil from the mesocarp. While the two names are often used interchangeably, palm oil is commonly used for food products due to its near-even balance of unsaturated and saturated fatty acids and its alpha- and beta-carotenes, while palm kernel oil is more commonly used in other products such as soaps and cosmetics and is less saturated relative to palm oil [77]. Red palm oil is a further differentiated oil and refers to palm oil with a high carotenoid content giving it a dark red colour.

E. guineensis树的果实可产出两类油脂：来自胚乳的棕榈仁油，以及来自中果皮的棕榈油。尽管这两个名称常被混用，但棕榈油因其不饱和与饱和脂肪酸比例接近均衡并含有α-和β-胡萝卜素，常用于食品；而棕榈仁油更多用于肥皂和化妆品等其他产品，其饱和度相对棕榈油较低 [77]。红棕榈油是另一种细分油品，指类胡萝卜素含量高而呈深红色的棕榈油。

Trace elements may be present in palm and palm kernel oil as a result of processing (including refining, manufacturing, storage, shipping and packaging) and processing equipment due to E. guineensis plant uptake from soils or from soil contamination on kernels (i.e., dust from harvesting on associated soils) [7,78]. Trace elements in palm oils may occur as complexed impurities and contribute to dietary trace nutrient intake, which may provide nutritional benefits or, in excessive quantities, may breach food safety standards and pose risks to human health when ingested [7,79]. Here, research on TEs in palm oils is reviewed. A summary of available data of TEs in palm and palm kernel oils is presented in Table 5.

棕榈油和棕榈仁油中的微量元素可能来源于加工过程（包括精炼、生产、储存、运输和包装）及加工设备，也可能源于E. guineensis植株从土壤中的吸收或果仁上的土壤污染（即收获时来自相关土壤的粉尘）[7,78]。棕榈油中的微量元素可能以络合杂质形式存在，并构成膳食微量营养素摄入的一部分，这可能带来营养益处，但若过量则可能违反食品安全标准，摄入后对人体健康构成风险 [7,79]。本节综述了棕榈油中微量元素的研究。棕榈油和棕榈仁油中微量元素现有数据汇总于表5。

Crude palm oil is extracted from the mesocarp of E. guineensis either by solvent (chemical) or physical (manual crushing of palm kernels) extraction [80]. It may then be further refined by rinsing with hot demineralised water; degumming with citric acid; adsorptive cleaning, bleaching, and filtering to remove TEs and other impurities; and deodorising to remove volatile compounds [7]. Non-uniform manufacturing processes can affect TE concentrations in palm oil. In an analysis of oil at all stages of the above refining process, Szydłowska-Czerniak et al. [7] found that refining removed 72%, 94% and 63% of Fe, Cu and Pb from crude palm oil, respectively. A more than three-fold increase in Pb was noted between the filtering and deodorising steps and attributed to contamination from the equipment used in this step of the refining process. Copper concentrations in crude palm oil (0.46 mg kg⁻¹) exceeded Polish standards of 0.40 mg kg⁻¹. However, the final product fell within the acceptable range of <0.10 mg kg⁻¹. No other exceedances of standards were noted by the authors. A similar study of the same TEs was conducted on Indonesian crude palm oil by Rossi et al. [81]. They concluded that using phosphoric rather than citric acid as a degumming agent increased Pb concentrations in degummed oil; however, concentrations of Cu and Pb in the fully refined product were less than the suggested limit of 0.1 mg kg⁻¹ [82]. These two studies demonstrate how non-uniform manufacturing processes impact the TE content of marketed palm oils.

粗棕榈油通过溶剂（化学）浸提或物理（人工压榨棕榈仁）压榨从E. guineensis中果皮中提取 [80]。随后可进一步精炼：用热去离子水冲洗；用柠檬酸脱胶；通过吸附净化、脱色和过滤去除微量元素及其他杂质；以及脱臭去除挥发性化合物 [7]。不统一的生产工艺会影响棕榈油中的微量元素浓度。Szydłowska-Czerniak et al. [7]对上述精炼过程各阶段的油样进行分析发现，精炼分别去除了粗棕榈油中72%、94%和63%的Fe、Cu和Pb。在过滤与脱臭步骤之间，Pb增加了三倍以上，这被归因于该精炼步骤所用设备的污染。粗棕榈油中的Cu浓度（0.46 mg kg⁻¹）超过了波兰标准0.40 mg kg⁻¹。但最终产品处于 <0.10 mg kg⁻¹的可接受范围内。作者未发现其他超标情况。Rossi et al. [81]对印度尼西亚粗棕榈油中相同的微量元素开展了类似研究。他们得出结论，使用磷酸而非柠檬酸作为脱胶剂会提高脱胶油中的Pb浓度；然而，完全精炼产品中Cu和Pb的浓度低于建议限值0.1 mg kg⁻¹ [82]。这两项研究说明了不统一的生产工艺如何影响市售棕榈油的微量元素含量。

Two studies by Chen et al. [83] and Chen et al. [84] determined As concentrations in refined and fractionated palm oils from Taiwan, with both studies reporting low As concentrations (≤0.025 mg kg⁻¹). Limits for As in oils have not yet been determined, and the toxicity risk depends on the type of As present (organic or inorganic) [85]. Australasian food standards set a limit of 1 mg kg⁻¹ total As for cereals and 0.5 mg kg⁻¹ for salt; however, limits are often set only for inorganic As due to its higher toxicity [86]. Consequently, research on As speciation in palm oils may be beneficial for the purpose of addressing the risk of As-toxicity.

Chen et al. [83]和Chen et al. [84]的两项研究测定了台湾精炼和分提棕榈油中的As浓度，两项研究均报道As浓度较低（≤0.025 mg kg⁻¹）。油脂中As的限值尚未确定，其毒性风险取决于As的存在形态（有机或无机）[85]。澳新食品标准规定谷物中总As限值为1 mg kg⁻¹，盐中为0.5 mg kg⁻¹；然而，由于无机As毒性更高，限值往往仅针对无机As设定 [86]。因此，开展棕榈油中As形态研究可能有助于应对As毒性风险。

Various studies have investigated elemental concentrations of Nigerian palm oil [87–90]. Collectively, Al, Cr, Mn, Fe, Co, Ni, Cu, Zn, As, Cd, Hg and Pb have been analysed using atomic absorption spectrometry methods. All elements were reported present at concentrations that posed no risk to human health according to standards set by Nigerian regulatory bodies; however, atomic absorption spectrometry may not be a sufficiently sensitive method for this analysis [91]. Further research analysing TEs in Nigerian palm oil using more analytically sensitive methods, e.g., optical emission spectrometry or mass spectrometry, would be beneficial.

多项研究调查了尼日利亚棕榈油中的元素浓度 [87–90]。这些研究共采用原子吸收光谱法分析了Al、Cr、Mn、Fe、Co、Ni、Cu、Zn、As、Cd、Hg和Pb。根据尼日利亚监管机构制定的标准，所有元素的报道浓度均未对人体健康构成风险；然而，原子吸收光谱法对于此类分析的灵敏度可能不足 [91]。采用灵敏度更高的分析方法（如发射光谱法或质谱法）进一步分析尼日利亚棕榈油中的微量元素将是有益的。

Two studies were identified which investigated TE concentrations in palm kernel oil [92,93]. Here, reported Al, Cl, V, Mn, Fe, Cu and Zn concentrations were comparable to those of palm oils in other studies (Table 5).

共找到两项调查棕榈仁油中微量元素浓度的研究 [92,93]。其中报道的Al、Cl、V、Mn、Fe、Cu和Zn浓度与其他研究中棕榈油的浓度相当（表5）。

While multiple studies have addressed TEs in Nigerian palm oils, there is a scarcity of research on palm kernel oil and oils from other countries, particularly Malaysia and Indonesia. This is significant since these countries produce almost 85% of the world’s traded palm oil supply [95]. Malaysian and Indonesian production soils differ from each other and from other palm-producing countries, and there are various methods of oil extraction used across different plantation types. There is little current knowledge on the risks or benefits of TEs in palm oil and palm kernel oil as a result of these differing soils, plantation types, and production practices in Southeast Asia.

尽管已有多项研究涉及尼日利亚棕榈油中的微量元素，但有关棕榈仁油以及其他国家（尤其是马来西亚和印度尼西亚）油脂的研究十分匮乏。这一点意义重大，因为这两个国家生产了全球贸易棕榈油供应量的近85% [95]。马来西亚和印度尼西亚的生产土壤彼此不同，也有别于其他棕榈生产国，且不同类型的种植园采用多种油脂提取方法。对于东南亚这些不同土壤、种植园类型和生产方式所导致的棕榈油和棕榈仁油中微量元素的风险或益处，目前了解甚少。

^a Nigeria, neutron activation analysis, number in brackets assumed to be standard deviation of the mean, number of samples not indicated [93]. ^b Nigeria [88]. ^c Nigeria [90]. ^d Nigeria, range of means, red palm oil [94]. ^e Nigeria, range of means [87]. ^f Nigeria, number in brackets assumed to be standard deviation of the mean, number of samples not indicated [92]. ^g Nigeria [89]. ^h Poland, number in brackets is standard deviation of the mean (n = 3) of final palm oil product after deodorising, analysed by inductively coupled plasma [7]. ⁱ Indonesia, steam refined oil [81]. ^j Taiwan [83]. ^k Taiwan [84].

^a 尼日利亚，中子活化分析，括号内数字假定为平均值的标准差，未注明样品数 [93]。^b 尼日利亚 [88]。^c 尼日利亚 [90]。^d 尼日利亚，均值范围，红棕榈油 [94]。^e 尼日利亚，均值范围 [87]。^f 尼日利亚，括号内数字假定为平均值的标准差，未注明样品数 [92]。^g 尼日利亚 [89]。^h 波兰，括号内数字为脱臭后棕榈油最终产品平均值的标准差（n = 3），采用电感耦合等离子体法分析 [7]。ⁱ 印度尼西亚，蒸汽精炼油 [81]。^j 台湾 [83]。^k 台湾 [84]。

5Trace Elements in Palm Kernel Expeller棕榈仁粕中的微量元素

Palm kernel expeller is the dry matter by-product of palm oil production, which is exported by manufacturing countries—primarily Indonesia and Malaysia—and utilised as a stockfeed in many Asian, European and Oceanic nations. Of these, New Zealand imports the largest amount of PKE annually, at 2,300,000 t in 2019 [96]. Although studies (and indeed importers) rarely differentiate between palm oils produced by physical and solvent extraction, Alimon [80] asserts that the latter leaves less oil in the PKE by-product (1–2%) compared to physical extraction (4–8%). Oil contents ranging up to 17.3% have been reported elsewhere [97]. Physical extraction is most commonly used as it is a more economical option [80]. As with palm oils, TEs may occur in PKE as a result of plant TE-uptake from soil, machinery and equipment used in manufacturing processes, and from soil contamination [7,78]. The TE content of PKE as a supplementary stockfeed has implications for animal and human health. Accordingly, Grace and Knowles [98] acknowledged that attention must be paid to the cumulative intake of minerals by animals from non-pasture-based feeds to ensure TE toxicity does not occur. Available information on PKE TE concentrations is presented in Table 6.

棕榈仁粕是棕榈油生产的干物质副产品，由生产国（主要是印度尼西亚和马来西亚）出口，并在许多亚洲、欧洲和大洋洲国家用作饲料。其中，新西兰每年进口的PKE数量最多，2019年达2,300,000 t [96]。尽管研究（乃至进口商）很少区分物理压榨和溶剂浸提生产的棕榈油，但Alimon [80]指出，与物理压榨（4–8%）相比，后者在PKE副产品中残留的油较少（1–2%）。另有报道油含量高达17.3% [97]。由于物理压榨更为经济，因此最常采用 [80]。与棕榈油一样，PKE中的微量元素可能来自植物对土壤微量元素的吸收、生产过程中使用的机械设备以及土壤污染 [7,78]。PKE作为补充饲料，其微量元素含量对动物和人体健康具有影响。因此，Grace and Knowles [98]指出，必须关注动物从非牧草饲料中累积摄入的矿物质，以确保不发生微量元素中毒。PKE微量元素浓度的现有信息列于表6。

Three studies could be identified which have investigated TE concentrations of PKE [80,99,100]. Of these, two reported TE concentrations within acceptable ranges, or below Maximum Tolerable Levels (MTLs), for animal feed [80,100]. These include Mn, Zn, Se and Mo at concentrations below 2000, 500, 5 and 5 mg kg⁻¹, respectively [101].

共找到三项调查PKE中微量元素浓度的研究 [80,99,100]。其中两项报道的微量元素浓度处于动物饲料的可接受范围内，或低于最大耐受水平（MTLs）[80,100]。这些元素包括Mn、Zn、Se和Mo，其浓度分别低于2000、500、5和5 mg kg⁻¹ [101]。

Copper and As have been reported at concentrations that exceed 50% of their MTLs of 40 (This MTL is for animals fed a diet of 1–2 mg kg⁻¹ Mo and 1500–2500 mg kg⁻¹ S: Cu may become toxic at lower concentrations if dietary Mo and S are below these levels) and 4 mg kg⁻¹, respectively [80,99,100]. Alimon [80] noted that Cu concentrations of PKE up to 28.9 mg kg⁻¹ exceeded ruminant requirements, and animals fed a diet of >50% PKE may develop Cu-toxicity symptoms. An ovine feed experiment on the occurrence of Cu-toxicity by Hair Bejo and Alimon [102] corroborates this point: all animals in PKE-fed groups not supplemented with Zn died before the study was completed due to Cu-toxicity from PKE, while those in Zn-supplemented and control groups survived. Thus, while high Cu concentrations in PKE can be a source of risk for livestock in receiving environments, this may be mitigated with appropriate TE management. Conversely, if managed correctly, the Cu content of PKE may provide a benefit to countries such as New Zealand, where background soil Cu concentrations are low, and farmers must supplement livestock at an expense [103].

据报道，Cu和As的浓度超过了其MTL（分别为40（该MTL适用于日粮中Mo为1–2 mg kg⁻¹、S为1500–2500 mg kg⁻¹的动物：若日粮中Mo和S低于这些水平，Cu可能在更低浓度下即产生毒性）和4 mg kg⁻¹）的50% [80,99,100]。Alimon [80]指出，PKE中高达28.9 mg kg⁻¹的Cu浓度超过了反刍动物的需求，饲喂PKE占比 >50%日粮的动物可能出现Cu中毒症状。Hair Bejo and Alimon [102]关于Cu中毒发生情况的绵羊饲喂试验印证了这一点：饲喂PKE且未补充Zn的各组动物均因PKE导致的Cu中毒而在研究结束前死亡，而补充Zn组和对照组的动物则存活。因此，尽管PKE中的高Cu浓度可对输入地的牲畜构成风险，但通过适当的微量元素管理可减轻这一风险。反之，若管理得当，PKE的Cu含量可能为新西兰等国家带来益处，因为这些国家土壤背景Cu浓度低，农民须花费成本为牲畜补充Cu [103]。

^a [100]. ^b [80]. ^c [99]. ^d [101]. ^e This value assumes a dietary Mo concentration of 1–2 mg kg⁻¹ and S concentration of 1500–2500 mg kg⁻¹. With less Mo and S in animals’ diets, Cu toxicity may occur at lower levels. ^f [104].

^a [100]。^b [80]。^c [99]。^d [101]。^e 该值假定日粮Mo浓度为1–2 mg kg⁻¹，S浓度为1500–2500 mg kg⁻¹。若动物日粮中Mo和S较少，Cu可能在更低水平下产生毒性。^f [104]。

Iron has been reported in PKE in concentrations up to 6130 mg kg⁻¹ [80]. This upper concentration range is >10-fold higher than is permissible in cattle feed (500 mg kg⁻¹ [101]). It is likely that this Fe is a result of contamination during manufacturing processes, as this concentration is far in excess of upper range kernel concentrations reported by Akpanabiatu et al. [71] (220 mg kg⁻¹) and average land plant Fe concentrations (140 mg kg⁻¹ [26]). Excessive Fe intake in bovines can decrease milk production and body weight, with minimum deleterious doses estimated below 30 mg kg⁻¹ day⁻¹ [105]. Thus, there is an apparent risk of TE-toxicity for animals fed PKE containing TEs of these concentrations.

据报道，PKE中Fe的浓度高达6130 mg kg⁻¹ [80]。该浓度上限比肉牛饲料允许值（500 mg kg⁻¹ [101]）高出10倍以上。这些Fe很可能来自生产过程中的污染，因为该浓度远超Akpanabiatu et al. [71]报道的果仁浓度上限（220 mg kg⁻¹）以及陆生植物的平均Fe浓度（140 mg kg⁻¹ [26]）。牛过量摄入Fe会降低产奶量和体重，估计最低有害剂量低于30 mg kg⁻¹ day⁻¹ [105]。因此，饲喂含此类浓度微量元素的PKE的动物显然存在微量元素中毒风险。

While attention has been given to Cu-toxicity risk in animals consuming PKE, other elements identified in the above-mentioned publications may also be of concern. In particular, Fe may be present in concentrations that pose risks to milk yield and animal health. Further research on the overall mineral composition of PKE would be beneficial, as there is a lack of data available on the concentrations of other non-essential biotoxic TEs, including Pb and Cd, which may be present in PKE due to their presence as impurities in phosphate fertilisers used in E. guineensis production [17,37]. Furthermore, there is a lack of research on PKE sourced from outside Malaysia and from different plantation types (including smallholder, community managed, government- and corporate-owned), whose management practices result in non-uniform application and accumulation of TEs in soil, plants and end-products [37]. Overall, there are scarce data available on the TE content of PKE, and filling this knowledge gap would be beneficial for all countries utilising this by-product in their agricultural systems by way of maintaining livestock well-being and soil nutrient status.

尽管动物食用PKE的Cu中毒风险已受到关注，但上述文献中涉及的其他元素也可能值得关注。特别是Fe的存在浓度可能对产奶量和动物健康构成风险。进一步研究PKE的整体矿物组成将是有益的，因为目前缺乏关于其他非必需生物毒性微量元素（包括Pb和Cd）浓度的数据，而这些元素可能因作为E. guineensis生产所用磷肥中的杂质而存在于PKE中 [17,37]。此外，缺乏对马来西亚以外来源以及不同类型种植园（包括小农户、社区管理、政府和企业所有）所产PKE的研究，这些种植园的管理方式导致微量元素在土壤、植物和终端产品中的施用和累积不均 [37]。总体而言，PKE微量元素含量的数据十分匮乏，填补这一知识空白将有助于所有在农业系统中利用该副产品的国家维护牲畜健康和土壤养分状况。

6Conclusions结论

This review has identified the elements of concern in E. guineensis production systems as Fe, Cu, Zn, Cd and As. Copper, Zn and Cd have been reported in production soils at elevated concentrations and may pose risks to production if allowed to accumulate past soil guideline values. These TEs are present and accumulate in E. guineensis production soils, likely as a result of phosphate fertiliser and Cu-fungicide use in plantations. Iron may be present in PKE in concentrations >10-fold higher than its MTL—likely as a result of contamination during PKE processing—while Cu and As have been reported to be in excess of 50% of their MTLs. Using PKE for animal fodder may present risks or a benefit to the agricultural systems of importing countries depending on what TEs are present and in what concentrations. There is a disparity between regions where E. guineensis is produced— namely Indonesia and Malaysia, and regions producing research on TEs in E. guineensis systems—most often Nigeria. The critical knowledge gaps concerning TEs in E. guineensis production systems are: data on the elemental composition of PKE; the concentrations of Cu, Zn, As and Cd in Southeast Asian production soils; and data on mercury across the entire production system, from soils to products. Future research should focus on a whole-systems analysis to determine the viability of E. guineensis production systems and identify appreciable risks to allow the development of mitigation strategies that may be applied at the plantation level and address the emerging issue of TE contamination.

本综述确定E. guineensis生产体系中需关注的元素为Fe、Cu、Zn、Cd和As。据报道，生产土壤中Cu、Zn和Cd的浓度较高，若任其累积超过土壤指导值，可能对生产构成风险。这些微量元素存在于E. guineensis生产土壤中并不断累积，很可能是种植园施用磷肥和铜基杀菌剂所致。PKE中Fe的浓度可能比其MTL高出10倍以上（很可能源于PKE加工过程中的污染），而Cu和As的报道浓度则超过其MTL的50%。将PKE用作动物饲料可能给进口国的农业系统带来风险或益处，这取决于所含微量元素的种类及其浓度。E. guineensis的主产区（即印度尼西亚和马来西亚）与开展E. guineensis体系微量元素研究的地区（最常见的是尼日利亚）之间存在不匹配。E. guineensis生产体系中微量元素的关键知识空白包括：PKE的元素组成数据；东南亚生产土壤中Cu、Zn、As和Cd的浓度；以及从土壤到产品整个生产体系中汞的数据。未来研究应侧重于全系统分析，以确定E. guineensis生产体系的可行性并识别显著风险，从而制定可在种植园层面实施的缓解策略，应对微量元素污染这一新问题。

Supplementary Materials: The following supporting information can be downloaded at: https: //www.mdpi.com/article/10.3390/su14084553/s1, Table S1: Rare earth element concentrations in Aceraceae species.

补充材料：以下支持信息可从 https: //www.mdpi.com/article/10.3390/su14084553/s1 下载，表S1：Aceraceae物种中的稀土元素浓度。

Author Contributions: H.T.-M.: Conceptualisation, Investigation, Writing—Original Draft. S.G.: Writing—Review and Editing, Supervision. B.R.: Writing—Review and Editing, Supervision. All authors have read and agreed to the published version of the manuscript.

作者贡献：H.T.-M.：构思、调查、撰写——初稿。S.G.：撰写——审阅与编辑、指导。B.R.：撰写——审阅与编辑、指导。所有作者均已阅读并同意本文的发表版本。

Funding: This work is derived from the Centre for Integrated Biowaste Research funded by Strategic Science Investment Funding from Ministry of Business, Innovation and Employment, New Zealand (contract C03×1701). The lead author gratefully acknowledges the receipt of a University of Canterbury Doctoral Scholarship.

基金资助：本研究源于新西兰商业、创新和就业部（Ministry of Business, Innovation and Employment）战略科学投资基金资助的综合生物废弃物研究中心（Centre for Integrated Biowaste Research）（合同号C03×1701）。第一作者衷心感谢坎特伯雷大学博士奖学金的资助。

Institutional Review Board Statement: Not applicable.

机构审查委员会声明：不适用。

Data Availability Statement: Not applicable.

数据可用性声明：不适用。

Acknowledgments: The authors would like to acknowledge the help of Clinton Webb in proofreading this article.

致谢：作者感谢Clinton Webb在本文校对方面提供的帮助。

Conflicts of Interest: The funders had no role in the design of the study; in the collection, analyses, or interpretation of data; in the writing of the manuscript, or in the decision to publish the results.

利益冲突：资助方未参与本研究的设计，数据的收集、分析或解释，稿件的撰写，以及发表结果的决定。

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